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SMBE 2016 Call for Satellite Meeting Proposals

In addition to supporting its annual meeting, SMBE Council will provide funds in aid of one or more workshops or small (with fewer than 100 participants) SATELLITE MEETINGS per calendar year, that number depending on total cost. In the past five years, SMBE has supported multiple satellite meetings on diverse topics (e.g., “Phylomedicine” 2012, “Eukaryotic Metagenomics” 2013, “Mechanisms of Protein Evolution II” 2013, “The Origin of Life” 2014, “Causes of Genome Evolution” 2014, “Phylogenomic Networks in Microbial Genome Evolution” 2014, “Investigating biological adaptation with NGS: data and models” 2015, “Mutation, Repair and Evolution” 2015, “Phylogenetics and Biodiversity” 2015, “Mechanisms of Protein Evolution III” 2015, “Genome Evolution in Pathogen Transmission and Disease” 2016, “Genetics of admixed populations” 2016, “RNA modification and its implication on adaptation and evolution” 2016).

SMBE is now calling for proposals for workshops/satellite meetings to be held between Fall 2016 and Fall 2017. Funds will be awarded on a competitive basis to members of the molecular evolution research community to run workshops/satellite meetings on an important, focused, and timely topic of their choice. The deadline for submission of proposals is May 15, 2016.

NEW: SMBE INTERDISCIPLINARY AND REGIONAL ACTIONS. In addition to supporting its annual meeting and satellite meetings, SMBE will promote interdisciplinary research and extend its actions worldwide by sponsoring (1) joint meetings with meetings of other societies; symposia or plenary lectures on molecular biology and evolution at meetings whose primary focus is not molecular evolution; (2) regional meetings outside the US, Europe, and Japan; (3) small regional meetings in the US, Europe, and Japan targeted for PhD students and postdocs with the purpose of helping them develop their communication skills and to facilitate networking. Funds will be awarded on a competitive basis to members of the molecular evolution research community to run all three types of actions. SMBE is now calling for proposals to be held between Fall 2016 and Fall 2017. The number of awards will depend on the quality of proposals and total cost. The deadline for submission of proposals is May 15, 2016.


• SMBE will provide financial support for up to 80% of the cost of each satellite meeting, up to maximum of $40,000 USD per meeting (most meetings are funded at $20,000-$30,000 each). SMBE will provide financial support for up to 80% of the cost for the joint and regional meetings, up to maximum of $25,000 USD per meeting (up to $10,000 USD for small regional meetings in the US, Europe, and Japan). SMBE will cover the cost of plenary lectures, up to a maximum of $3,000 USD per lecture. A detailed projected budget, including the expected number of participants, travel/food/lodging costs, and registration fees must be submitted with the application.

At least one of the organizers must be a member of SMBE. Current SMBE Council members, or members who have rotated-off Council in the last calendar year, are not eligible to serve as meeting organizers or co-organizers.

• For satellite meetings, funds will be awarded on a competitive basis to members of the molecular evolution research community that propose an important, focused, and timely topic. Topics not well represented in symposia of SMBE annual meetings will be favored over those that are already well represented at the annual meetings or previous SMBE satellite meetings. For Interdisciplinary and Regional actions, meetings/symposia/lectures will be selected based on the scientific importance, timeliness and anticipated impact on the fields of molecular biology, genome biology, and evolution.

·   Proposals are encouraged to include details for plans about the recruitment of speakers and participants that will ensure broad representation across SMBE membership, including gender and geographical location. Proposals for meetings to be organized in geographical areas that have been traditionally under-represented in SMBE meetings (annual or satellite) are especially encouraged.

• Proposals will be received and reviewed by the SMBE Satellite Workshop Committee and SMBE Interdisciplinary and Regional Actions Committee. Each Committee will consist of four individuals: one SMBE Council Member (who will also serve as Chair) and three other members of SMBE. The committees will make a recommendation to SMBE Council, whose decision is final. The committees or SMBE Council may decide not to support any meeting in any particular year.

• Events will be named “SMBE Satellite Meeting on XYZ”, or “SMBE Interdisciplinary Meeting/Symposium/Lecture” and “SMBE Regional Meeting in XYZ(Geographic Location)”. Meeting organizers should host a website for the meeting that highlights the main theme as well as program, including the speaker list. This website should stay active for at least 3 years after the meeting date. Symposium and lecture organizers should provide a link to be advertised on the SMBE webpage. The sponsorship of the SMBE must be mentioned in all pre-meeting publicity and in the meeting programme.

• The satellite meeting/workshop and a regional meeting must be a standalone event. It should not form a symposium or other part of a larger meeting. It should not immediately follow or precede any other meeting.

• Organizers will be required to submit a copy of the final workshop/symposium/meeting program and a short (~2 page) summary of the workshop/symposium/meeting highlights to SMBE Council within 3 months of the event.  The summary for satellite meetings should be sent to Kateryna Makova (kdm16@psu.edu), and for Interdisciplinary and Regional Actions – to Maud Tenaillon (tenaillon@moulon.inra.fr).

Instructions for proposals

Satellite meeting / workshop proposals should be sent by email to the Chair of the SMBE Satellite Workshop Committee Kateryna Makova (kdm16@psu.edu). Interdisciplinary and Regional Actions proposals should be sent by email to the Chair of the SMBE Interdisciplinary Regional Actions Committee Maud Tenaillon (tenaillon@moulon.inra.fr).

The deadline for submission of proposals is May 15, 2016.

1. Provide the name(s) and full contact information for all organizer(s) and institution(s) involved. Universities/ organizations providing additional financial support, if involved, should also be listed. If additional funding is being simultaneously applied for, please state the status of that request as well.

2. Workshop/action summary  (4 single-spaced pages max, 1 page max for a lecture). Describe the scientific rationale for your proposed workshop. In doing so, be sure to clearly state (1) the importance and timeliness of the topic, (2) the anticipated short-term and long-term impacts of your meeting or action on the fields of molecular biology, genome biology, and evolution, (3) the proposed structure of your workshop/meeting or action (e.g., lectures only, lectures + hands-on training sessions, contributed talks, poster sessions, etc.), (4) an indicative list of proposed invited speakers; (5) for satellite meetings only: why a workshop/small meeting format is preferable to a symposium at the SMBE annual meeting; (6) for interdisciplinary actions only: the relevance of mixing communities (for joint meetings, symposia and plenary lectures at non-evolution meetings); (7) for regional actions outside the US, Europe, and Japan only: the relevance of promoting actions in specific regions; (8) for small regional actions in the US, Europe, and Japan only: the extent and nature of student/postdoctoral fellow involvement.

3. Financial summary. Please summarize your financial request, including estimated total budget, registration costs (if any), travel support for speakers / trainees, and details of non-SMBE funds to be used.

  • Monday, March 21, 2016
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The Society for Molecular Biology and Evolution is an international organization whose goals are to provide facilities for association and communication among molecular evolutionists and to further the goals of molecular evolution, as well as its practitioners and teachers. In order to accomplish these goals, the Society publishes two peer-reviewed journals, Molecular Biology and Evolution and Genome Biology and Evolution. The Society sponsors an annual meeting, as well as smaller satellite meetings or workshop on important, focused, and timely topics. It also confers honors and awards to students and researchers.

SMBE 2019

We are delighted to announce that the SMBE 2019 Meeting will be taking place in Manchester, United Kingdom. The Meeting will be held at the state of the art Manchester Central venue.

The programme will provide plenty of opportunities for you to submit your work for consideration as a symposium, oral or poster presentation.

Full details on registration fees, accommodation and exhibition opportunities will be made available in due course. Please do make a note of the key dates included below.

More information can be found HERE


SMBE is a member of the Scientific Society Publisher Alliance

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MBE | Most Read

Molecular Biology and Evolution

The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion

Tue, 06 Aug 2019 00:00:00 GMT

The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here, we report an extensive analysis of the M. exilis genome to address this question. Unexpectedly, we find that M. exilis genome structure and content is similar in complexity to other eukaryotes and less “reduced” than genomes of some other protists from the Metamonada group to which it belongs. Furthermore, the predicted cytoskeletal systems, the organization of endomembrane systems, and biosynthetic pathways also display canonical eukaryotic complexity. The only apparent preadaptation that permitted the loss of mitochondria was the acquisition of the SUF system for Fe–S cluster assembly and the loss of glycine cleavage system. Changes in other systems, including in amino acid metabolism and oxidative stress response, were coincident with the loss of mitochondria but are likely adaptations to the microaerophilic and endobiotic niche rather than the mitochondrial loss per se. Apart from the lack of mitochondria and peroxisomes, we show that M. exilis is a fully elaborated eukaryotic cell that is a promising model system in which eukaryotic cell biology can be investigated in the absence of mitochondria.

Adaptive Changes in Hemoglobin Function in High-Altitude Tibetan Canids Were Derived via Gene Conversion and Introgression

Tue, 30 Jul 2019 00:00:00 GMT

A key question in evolutionary biology concerns the relative importance of different sources of adaptive genetic variation, such as de novo mutations, standing variation, and introgressive hybridization. A corollary question concerns how allelic variants derived from these different sources may influence the molecular basis of phenotypic adaptation. Here, we use a protein-engineering approach to examine the phenotypic effect of putatively adaptive hemoglobin (Hb) mutations in the high-altitude Tibetan wolf that were selectively introgressed into the Tibetan mastiff, a high-altitude dog breed that is renowned for its hypoxia tolerance. Experiments revealed that the introgressed coding variants confer an increased Hb–O2 affinity in conjunction with an enhanced Bohr effect. We also document that affinity-enhancing mutations in the β-globin gene of Tibetan wolf were originally derived via interparalog gene conversion from a tandemly linked β-globin pseudogene. Thus, affinity-enhancing mutations were introduced into the β-globin gene of Tibetan wolf via one form of intragenomic lateral transfer (ectopic gene conversion) and were subsequently introduced into the Tibetan mastiff genome via a second form of lateral transfer (introgression). Site-directed mutagenesis experiments revealed that the increased Hb–O2 affinity requires a specific two-site combination of amino acid replacements, suggesting that the molecular underpinnings of Hb adaptation in Tibetan mastiff (involving mutations that arose in a nonexpressed gene and which originally fixed in Tibetan wolf) may be qualitatively distinct from functionally similar changes in protein function that could have evolved via sequential fixation of de novo mutations during the breed’s relatively short duration of residency at high altitude.

Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals

Tue, 16 Jul 2019 00:00:00 GMT

Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.

Epimutations in Developmental Genes Underlie the Onset of Domestication in Farmed European Sea Bass

Wed, 10 Jul 2019 00:00:00 GMT

Domestication of wild animals induces a set of phenotypic characteristics collectively known as the domestication syndrome. However, how this syndrome emerges is still not clear. Recently, the neural crest cell deficit hypothesis proposed that it is generated by a mildly disrupted neural crest cell developmental program, but clear support is lacking due to the difficulties of distinguishing pure domestication effects from preexisting genetic differences between farmed and wild mammals and birds. Here, we use a farmed fish as model to investigate the role of persistent changes in DNA methylation (epimutations) in the process of domestication. We show that early domesticates of sea bass, with no genetic differences with wild counterparts, contain epimutations in tissues with different embryonic origins. About one fifth of epimutations that persist into adulthood are established by the time of gastrulation and affect genes involved in developmental processes that are expressed in embryonic structures, including the neural crest. Some of these genes are differentially expressed in sea bass with lower jaw malformations, a key feature of domestication syndrome. Interestingly, these epimutations significantly overlap with cytosine-to-thymine polymorphisms after 25 years of selective breeding. Furthermore, epimutated genes coincide with genes under positive selection in other domesticates. We argue that the initial stages of domestication include dynamic alterations in DNA methylation of developmental genes that affect the neural crest. Our results indicate a role for epimutations during the beginning of domestication that could be fixed as genetic variants and suggest a conserved molecular process to explain Darwin’s domestication syndrome across vertebrates.

Recurrent Losses and Rapid Evolution of the Condensin II Complex in Insects

Thu, 04 Jul 2019 00:00:00 GMT

Condensins play a crucial role in the organization of genetic material by compacting and disentangling chromosomes. Based on studies in a few model organisms, the condensins I and II complexes are considered to have distinct functions, with the condensin II complex playing a role in meiosis and somatic pairing of homologous chromosomes in Drosophila. Intriguingly, the Cap-G2 subunit of condensin II is absent in Drosophila melanogaster, and this loss may be related to the high levels of chromosome pairing seen in flies. Here, we find that all three non-SMC subunits of condensin II (Cap-G2, Cap-D3, and Cap-H2) have been repeatedly and independently lost in taxa representing multiple insect orders, with some taxa lacking all three. We also find that all non-Dipteran insects display near-uniform low-pairing levels regardless of their condensin II complex composition, suggesting that some key aspects of genome organization are robust to condensin II subunit losses. Finally, we observe consistent signatures of positive selection in condensin subunits across flies and mammals. These findings suggest that these ancient complexes are far more evolutionarily labile than previously suspected, and are at the crossroads of several forms of genomic conflicts. Our results raise fundamental questions about the specific functions of the two condensin complexes in taxa that have experienced subunit losses, and open the door to further investigations to elucidate the diversity of molecular mechanisms that underlie genome organization across various life forms.

Skeletal Mineralization in Association with Type X Collagen Expression Is an Ancestral Feature for Jawed Vertebrates

Thu, 04 Jul 2019 00:00:00 GMT

In order to characterize the molecular bases of mineralizing cell evolution, we targeted type X collagen, a nonfibrillar network forming collagen encoded by the Col10a1 gene. It is involved in the process of endochondral ossification in ray-finned fishes and tetrapods (Osteichthyes), but until now unknown in cartilaginous fishes (Chondrichthyes). We show that holocephalans and elasmobranchs have respectively five and six tandemly duplicated Col10a1 gene copies that display conserved genomic synteny with osteichthyan Col10a1 genes. All Col10a1 genes in the catshark Scyliorhinus canicula are expressed in ameloblasts and/or odontoblasts of teeth and scales, during the stages of extracellular matrix protein secretion and mineralization. Only one duplicate is expressed in the endoskeletal (vertebral) mineralizing tissues. We also show that the expression of type X collagen is present in teeth of two osteichthyans, the zebrafish Danio rerio and the western clawed frog Xenopus tropicalis, indicating an ancestral jawed vertebrate involvement of type X collagen in odontode formation. Our findings push the origin of Col10a1 gene prior to the divergence of osteichthyans and chondrichthyans, and demonstrate its ancestral association with mineralization of both the odontode skeleton and the endoskeleton.

Ancient Hybridization and Adaptive Introgression of an Invadolysin Gene in Schistosome Parasites

Thu, 27 Jun 2019 00:00:00 GMT

Introgression among parasite species has the potential to transfer traits of biomedical importance across species boundaries. The parasitic blood fluke Schistosoma haematobium causes urogenital schistosomiasis in humans across sub-Saharan Africa. Hybridization with other schistosome species is assumed to occur commonly, because genetic crosses between S. haematobium and livestock schistosomes, including S. bovis, can be staged in the laboratory, and sequencing of mtDNA and rDNA amplified from microscopic miracidia larvae frequently reveals markers from different species. However, the frequency, direction, age, and genomic consequences of hybridization are unknown. We hatched miracidia from eggs and sequenced the exomes from 96 individual S. haematobium miracidia from infected patients from Niger and the Zanzibar archipelago. These data revealed no evidence for contemporary hybridization between S. bovis and S. haematobium in our samples. However, all Nigerien S. haematobium genomes sampled show hybrid ancestry, with 3.3–8.2% of their nuclear genomes derived from S. bovis, providing evidence of an ancient introgression event that occurred at least 108–613 generations ago. Some S. bovis-derived alleles have spread to high frequency or reached fixation and show strong signatures of directional selection; the strongest signal spans a single gene in the invadolysin gene family (Chr. 4). Our results suggest that S. bovis/S. haematobium hybridization occurs rarely but demonstrate profound consequences of ancient introgression from a livestock parasite into the genome of S. haematobium, the most prevalent schistosome species infecting humans.

Advances and Applications in the Quest for Orthologs

Thu, 27 Jun 2019 00:00:00 GMT

Gene families evolve by the processes of speciation (creating orthologs), gene duplication (paralogs), and horizontal gene transfer (xenologs), in addition to sequence divergence and gene loss. Orthologs in particular play an essential role in comparative genomics and phylogenomic analyses. With the continued sequencing of organisms across the tree of life, the data are available to reconstruct the unique evolutionary histories of tens of thousands of gene families. Accurate reconstruction of these histories, however, is a challenging computational problem, and the focus of the Quest for Orthologs Consortium. We review the recent advances and outstanding challenges in this field, as revealed at a symposium and meeting held at the University of Southern California in 2017. Key advances have been made both at the level of orthology algorithm development and with respect to coordination across the community of algorithm developers and orthology end-users. Applications spanned a broad range, including gene function prediction, phylostratigraphy, genome evolution, and phylogenomics. The meetings highlighted the increasing use of meta-analyses integrating results from multiple different algorithms, and discussed ongoing challenges in orthology inference as well as the next steps toward improvement and integration of orthology resources.

Mutational and Selective Processes Involved in Evolution during Bacterial Range Expansions

Wed, 26 Jun 2019 00:00:00 GMT

Bacterial populations have been shown to accumulate deleterious mutations during spatial expansions that overall decrease their fitness and ability to grow. However, it is unclear if and how they can respond to selection in face of this mutation load. We examine here if artificial selection can counteract the negative effects of range expansions. We examined the molecular evolution of 20 mutator lines selected for fast expansions (SEL) and compared them to 20 other mutator lines freely expanding without artificial selection (CONTROL). We find that the colony size of all 20 SEL lines have increased relative to the ancestral lines, unlike CONTROL lines, showing that enough beneficial mutations are produced during spatial expansions to counteract the negative effect of expansion load. Importantly, SEL and CONTROL lines have similar numbers of mutations indicating that they evolved for the same number of generations and that increased fitness is not due to a purging of deleterious mutations. We find that loss of function mutations better explain the increased colony size of SEL lines than nonsynonymous mutations or a combination of the two. Interestingly, most loss of function mutations are found in simple sequence repeats (SSRs) located in genes involved in gene regulation and gene expression. We postulate that such potentially reversible mutations could play a major role in the rapid adaptation of bacteria to changing environmental conditions by shutting down expensive genes and adjusting gene expression.

Horizontal Transfer of Bacterial Cytolethal Distending Toxin B Genes to Insects

Tue, 25 Jun 2019 00:00:00 GMT

Horizontal gene transfer events have played a major role in the evolution of microbial species, but their importance in animals is less clear. Here, we report horizontal gene transfer of cytolethal distending toxin B (cdtB), prokaryotic genes encoding eukaryote-targeting DNase I toxins, into the genomes of vinegar flies (Diptera: Drosophilidae) and aphids (Hemiptera: Aphididae). We found insect-encoded cdtB genes are most closely related to orthologs from bacteriophage that infect Candidatus Hamiltonella defensa, a bacterial mutualistic symbiont of aphids that confers resistance to parasitoid wasps. In drosophilids, cdtB orthologs are highly expressed during the parasitoid-prone larval stage and encode a protein with ancestral DNase activity. We show that cdtB has been domesticated by diverse insects and hypothesize that it functions in defense against their natural enemies.

Antibiotic Resistance Evolution Is Contingent on the Quorum-Sensing Response in Pseudomonas aeruginosa

Sat, 22 Jun 2019 00:00:00 GMT

Different works have explored independently the evolution toward antibiotic resistance and the role of eco-adaptive mutations in the adaptation to a new habitat (as the infected host) of bacterial pathogens. However, knowledge about the connection between both processes is still limited. We address this issue by comparing the evolutionary trajectories toward antibiotic resistance of a Pseudomonas aeruginosa lasR defective mutant and its parental wild-type strain, when growing in presence of two ribosome-targeting antibiotics. Quorum-sensing lasR defective mutants are selected in P. aeruginosa populations causing chronic infections. Further, we observed they are also selected in vitro as a first adaptation for growing in culture medium. By using experimental evolution and whole-genome sequencing, we found that the evolutionary trajectories of P. aeruginosa in presence of these antibiotics are different in lasR defective and in wild-type backgrounds, both at the phenotypic and the genotypic levels. Recreation of a set of mutants in both genomic backgrounds (either wild type or lasR defective) allowed us to determine the existence of negative epistatic interactions between lasR and antibiotic resistance determinants. These epistatic interactions could lead to mutual contingency in the evolution of antibiotic resistance when P. aeruginosa colonizes a new habitat in presence of antibiotics. If lasR mutants are selected first, this would constraint antibiotic resistance evolution. Conversely, when resistance mutations (at least those studied in the present work) are selected, lasR mutants may not be selected in presence of antibiotics. These results underlie the importance of contingency and epistatic interactions in modulating antibiotic resistance evolution.

Fierce Selection and Interference in B-Cell Repertoire Response to Chronic HIV-1

Tue, 18 Jun 2019 00:00:00 GMT

During chronic infection, HIV-1 engages in a rapid coevolutionary arms race with the host’s adaptive immune system. While it is clear that HIV exerts strong selection on the adaptive immune system, the characteristics of the somatic evolution that shape the immune response are still unknown. Traditional population genetics methods fail to distinguish chronic immune response from healthy repertoire evolution. Here, we infer the evolutionary modes of B-cell repertoires and identify complex dynamics with a constant production of better B-cell receptor (BCR) mutants that compete, maintaining large clonal diversity and potentially slowing down adaptation. A substantial fraction of mutations that rise to high frequencies in pathogen-engaging CDRs of BCRs are beneficial, in contrast to many such changes in structurally relevant frameworks that are deleterious and circulate by hitchhiking. We identify a pattern where BCRs in patients who experience larger viral expansions undergo stronger selection with a rapid turnover of beneficial mutations due to clonal interference in their CDR3 regions. Using population genetics modeling, we show that the extinction of these beneficial mutations can be attributed to the rise of competing beneficial alleles and clonal interference. The picture is of a dynamic repertoire, where better clones may be outcompeted by new mutants before they fix.

Identifying Clusters of High Confidence Homologies in Multiple Sequence Alignments

Tue, 18 Jun 2019 00:00:00 GMT

Multiple sequence alignment (MSA) is ubiquitous in evolution and bioinformatics. MSAs are usually taken to be a known and fixed quantity on which to perform downstream analysis despite extensive evidence that MSA accuracy and uncertainty affect results. These errors are known to cause a wide range of problems for downstream evolutionary inference, ranging from false inference of positive selection to long branch attraction artifacts. The most popular approach to dealing with this problem is to remove (filter) specific columns in the MSA that are thought to be prone to error. Although popular, this approach has had mixed success and several studies have even suggested that filtering might be detrimental to phylogenetic studies. We present a graph-based clustering method to address MSA uncertainty and error in the software Divvier (available at https://github.com/simonwhelan/Divvier), which uses a probabilistic model to identify clusters of characters that have strong statistical evidence of shared homology. These clusters can then be used to either filter characters from the MSA (partial filtering) or represent each of the clusters in a new column (divvying). We validate Divvier through its performance on real and simulated benchmarks, finding Divvier substantially outperforms existing filtering software by retaining more true pairwise homologies calls and removing more false positive pairwise homologies. We also find that Divvier, in contrast to other filtering tools, can alleviate long branch attraction artifacts induced by MSA and reduces the variation in tree estimates caused by MSA uncertainty.

Recombination-Aware Phylogenomics Reveals the Structured Genomic Landscape of Hybridizing Cat Species

Fri, 14 Jun 2019 00:00:00 GMT

Current phylogenomic approaches implicitly assume that the predominant phylogenetic signal within a genome reflects the true evolutionary history of organisms, without assessing the confounding effects of postspeciation gene flow that can produce a mosaic of phylogenetic signals that interact with recombinational variation. Here, we tested the validity of this assumption with a phylogenomic analysis of 27 species of the cat family, assessing local effects of recombination rate on species tree inference and divergence time estimation across their genomes. We found that the prevailing phylogenetic signal within the autosomes is not always representative of the most probable speciation history, due to ancient hybridization throughout felid evolution. Instead, phylogenetic signal was concentrated within regions of low recombination, and notably enriched within large X chromosome recombination cold spots that exhibited recurrent patterns of strong genetic differentiation and selective sweeps across mammalian orders. By contrast, regions of high recombination were enriched for signatures of ancient gene flow, and these sequences inflated crown-lineage divergence times by ∼40%. We conclude that existing phylogenomic approaches to infer the Tree of Life may be highly misleading without considering the genomic architecture of phylogenetic signal relative to recombination rate and its interplay with historical hybridization.

Rapid Evolution of Gained Essential Developmental Functions of a Young Gene via Interactions with Other Essential Genes

Tue, 11 Jun 2019 00:00:00 GMT

New genes are of recent origin and only present in a subset of species in a phylogeny. Accumulated evidence suggests that new genes, like old genes that are conserved across species, can also take on important functions and be essential for the survival and reproductive success of organisms. Although there are detailed analyses of the mechanisms underlying new genes’ gaining fertility functions, how new genes rapidly become essential for viability remains unclear. We focused on a young retro-duplicated gene (CG7804, which we named Cocoon) in Drosophila that originated between 4 and 10 Ma. We found that, unlike its evolutionarily conserved parental gene, Cocoon has evolved under positive selection and accumulated many amino acid differences at functional sites from the parental gene. Despite its young age, Cocoon is essential for the survival of Drosophila melanogaster at multiple developmental stages, including the critical embryonic stage, and its expression is essential in different tissues from those of its parental gene. Functional genomic analyses found that Cocoon acquired unique DNA-binding sites and has a contrasting effect on gene expression to that of its parental gene. Importantly, Cocoon binding predominantly locates at genes that have other essential functions and/or have multiple gene–gene interactions, suggesting that Cocoon acquired novel essential function to survival through forming interactions that have large impacts on the gene interaction network. Our study is an important step toward deciphering the evolutionary trajectory by which new genes functionally diverge from parental genes and become essential.

DNA Methylation Changes in the Sperm of Captive-Reared Fish: A Route to Epigenetic Introgression in Wild Populations

Mon, 10 Jun 2019 00:00:00 GMT

Interbreeding between hatchery-reared and wild fish, through deliberate stocking or escapes from fish farms, can result in rapid phenotypic and gene expression changes in hybrids, but the underlying mechanisms are unknown. We assessed if one generation of captive breeding was sufficient to generate inter- and/or transgenerational epigenetic modifications in Atlantic salmon. We found that the sperm of wild and captive-reared males differed in methylated regions consistent with early epigenetic signatures of domestication. Some of the epigenetic marks that differed between hatchery and wild males affected genes related to transcription, neural development, olfaction, and aggression, and were maintained in the offspring beyond developmental reprogramming. Our findings suggest that rearing in captivity may trigger epigenetic modifications in the sperm of hatchery fish that could explain the rapid phenotypic and genetic changes observed among hybrid fish. Epigenetic introgression via fish sperm represents a previously unappreciated mechanism that could compromise locally adapted fish populations.

Gene Family Evolution in the Pea Aphid Based on Chromosome-Level Genome Assembly

Fri, 07 Jun 2019 00:00:00 GMT

Genome structural variations, including duplications, deletions, insertions, and inversions, are central in the evolution of eukaryotic genomes. However, structural variations present challenges for high-quality genome assembly, hampering efforts to understand the evolution of gene families and genome architecture. An example is the genome of the pea aphid (Acyrthosiphon pisum) for which the current assembly is composed of thousands of short scaffolds, many of which are known to be misassembled. Here, we present an improved version of the A. pisum genome based on the use of two long-range proximity ligation methods. The new assembly contains four long scaffolds (40–170 Mb), corresponding to the three autosomes and the X chromosome of A. pisum, and encompassing 86% of the new assembly. Assembly accuracy is supported by several quality assessments. Using this assembly, we identify the chromosomal locations and relative ages of duplication events, and the locations of horizontally acquired genes. The improved assembly illuminates the mode of gene family evolution by providing proximity information between paralogs. By estimating nucleotide polymorphism and coverage depth from resequencing data, we determined that many short scaffolds not assembling to chromosomes represent hemizygous regions, which are especially frequent on the highly repetitive X chromosome. Aligning the X-linked aphicarus region, responsible for male wing dimorphism, to the new assembly revealed a 50-kb deletion that cosegregates with the winged male phenotype in some clones. These results show that long-range scaffolding methods can substantially improve assemblies of repetitive genomes and facilitate study of gene family evolution and structural variation.

Coalescent Theory of Migration Network Motifs

Tue, 04 Jun 2019 00:00:00 GMT

Natural populations display a variety of spatial arrangements, each potentially with a distinctive impact on genetic diversity and genetic differentiation among subpopulations. Although the spatial arrangement of populations can lead to intricate migration networks, theoretical developments have focused mainly on a small subset of such networks, emphasizing the island-migration and stepping-stone models. In this study, we investigate all small network motifs: the set of all possible migration networks among populations subdivided into at most four subpopulations. For each motif, we use coalescent theory to derive expectations for three quantities that describe genetic variation: nucleotide diversity, FST, and half-time to equilibrium diversity. We describe the impact of network properties on these quantities, finding that motifs with a high mean node degree have the largest nucleotide diversity and the longest time to equilibrium, whereas motifs with low density have the largest FST. In addition, we show that the motifs whose pattern of variation is most strongly influenced by loss of a connection or a subpopulation are those that can be split easily into disconnected components. We illustrate our results using two example data sets—sky island birds of genus Sholicola and Indian tigers—identifying disturbance scenarios that produce the greatest reduction in genetic diversity; for tigers, we also compare the benefits of two assisted gene flow scenarios. Our results have consequences for understanding the effect of geography on genetic diversity, and they can assist in designing strategies to alter population migration networks toward maximizing genetic variation in the context of conservation of endangered species.

The Epigenetic Signature of Colonizing New Environments in Anolis Lizards

Thu, 30 May 2019 00:00:00 GMT

Founder populations often show rapid divergence from source populations after colonizing new environments. Epigenetic modifications can mediate phenotypic responses to environmental change and may be an important mechanism promoting rapid differentiation in founder populations. Whereas many long-term studies have explored the extent to which divergence between source and founder populations is genetically heritable versus plastic, the role of epigenetic processes during colonization remains unclear. To investigate epigenetic modifications in founding populations, we experimentally colonized eight small Caribbean islands with brown anole lizards (Anolis sagrei) from a common source population. We then quantitatively measured genome-wide DNA methylation in liver tissue using reduced representation bisulfite sequencing of individuals transplanted onto islands with high- versus low-habitat quality. We found that lizard sex and habitat quality explained a significant proportion of epigenetic variation. Differentially methylated cytosines mapped to genes that encode proteins with functions likely to be relevant to habitat change (e.g., signal transduction, immune response, circadian rhythm). This study provides experimental evidence of a relationship between epigenetic responses and the earliest stages of colonization of novel environments in nature and suggests that habitat quality influences the nature of these epigenetic modifications.

Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee

Wed, 29 May 2019 00:00:00 GMT

Social insect genomes exhibit the highest rates of crossing over observed in plants and animals. The evolutionary causes of these extreme rates are unknown. Insight can be gained by comparing recombination rate variation across the genomes of related social and solitary insects. Here, we compare the genomic recombination landscape of the highly social honey bee, Apis mellifera, with the solitary alfalfa leafcutter bee, Megachile rotundata, by analyzing patterns of linkage disequilibrium in population-scale genome sequencing data. We infer that average recombination rates are extremely elevated in A. mellifera compared with M. rotundata. However, our results indicate that similar factors control the distribution of crossovers in the genomes of both species. Recombination rate is significantly reduced in coding regions in both species, with genes inferred to be germline methylated having particularly low rates. Genes with worker-biased patterns of expression in A. mellifera and their orthologs in M. rotundata have higher than average recombination rates in both species, suggesting that selection for higher diversity in genes involved in worker caste functions in social taxa is not the explanation for these elevated rates. Furthermore, we find no evidence that recombination has modulated the efficacy of selection among genes during bee evolution, which does not support the hypothesis that high recombination rates facilitated positive selection for new functions in social insects. Our results indicate that the evolution of sociality in insects likely entailed selection on modifiers that increased recombination rates genome wide, but that the genomic recombination landscape is determined by the same factors.

Joint Maximum Likelihood of Phylogeny and Ancestral States Is Not Consistent

Thu, 23 May 2019 00:00:00 GMT

Maximum likelihood estimation in phylogenetics requires a means of handling unknown ancestral states. Classical maximum likelihood averages over these unknown intermediate states, leading to provably consistent estimation of the topology and continuous model parameters. Recently, a computationally efficient approach has been proposed to jointly maximize over these unknown states and phylogenetic parameters. Although this method of joint maximum likelihood estimation can obtain estimates more quickly, its properties as an estimator are not yet clear. In this article, we show that this method of jointly estimating phylogenetic parameters along with ancestral states is not consistent in general. We find a sizeable region of parameter space that generates data on a four-taxon tree for which this joint method estimates the internal branch length to be exactly zero, even in the limit of infinite-length sequences. More generally, we show that this joint method only estimates branch lengths correctly on a set of measure zero. We show empirically that branch length estimates are systematically biased downward, even for short branches.

Elucidation of Codon Usage Signatures across the Domains of Life

Mon, 20 May 2019 00:00:00 GMT

Because of the degeneracy of the genetic code, multiple codons are translated into the same amino acid. Despite being “synonymous,” these codons are not equally used. Selective pressures are thought to drive the choice among synonymous codons within a genome, while GC content, which is typically attributed to mutational drift, is the major determinant of variation across species. Here, we find that in addition to GC content, interspecies codon usage signatures can also be detected. More specifically, we show that a single amino acid, arginine, is the major contributor to codon usage bias differences across domains of life. We then exploit this finding and show that domain-specific codon bias signatures can be used to classify a given sequence into its corresponding domain of life with high accuracy. We then wondered whether the inclusion of codon usage codon autocorrelation patterns, which reflects the nonrandom distribution of codon occurrences throughout a transcript, might improve the classification performance of our algorithm. However, we find that autocorrelation patterns are not domain-specific, and surprisingly, are unrelated to tRNA reusage, in contrast to previous reports. Instead, our results suggest that codon autocorrelation patterns are a by-product of codon optimality throughout a sequence, where highly expressed genes display autocorrelated “optimal” codons, whereas lowly expressed genes display autocorrelated “nonoptimal” codons.

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Genome Biology & Evolution

Complete Genome Sequence of the Biocontrol Agent Bacillus velezensis UFLA258 and Its Comparison with Related Species: Diversity within the Commons

Thu, 03 Oct 2019 00:00:00 GMT

In this study, the full genome sequence of Bacillus velezensis strain UFLA258, a biological control agent of plant pathogens was obtained, assembled, and annotated. With a comparative genomics approach, in silico analyses of all complete genomes of B. velezensis and closely related species available in the database were performed. The genome of B. velezensis UFLA258 consisted of a single circular chromosome of 3.95 Mb in length, with a mean GC content of 46.69%. It contained 3,949 genes encoding proteins and 27 RNA genes. Analyses based on Average Nucleotide Identity and Digital DNA–DNA Hybridization and a phylogeny with complete sequences of the rpoB gene confirmed that 19 strains deposited in the database as Bacillus amyloliquefaciens were in fact B. velezensis. In total, 115 genomes were analyzed and taxonomically classified as follows: 105 were B. velezensis, 9 were B. amyloliquefaciens, and 1 was Bacillus siamensis. Although these species are phylogenetically close, the combined analyses of several genomic characteristics, such as the presence of biosynthetic genes encoding secondary metabolites, CRISPr/Cas arrays, Average Nucleotide Identity and Digital DNA–DNA Hybridization, and other information on the strains, including isolation source, allowed their unequivocal classification. This genomic analysis expands our knowledge about the closely related species, B. velezensis, B. amyloliquefaciens, and B. siamensis, with emphasis on their taxonomical status.

Genome of the Parasitoid Wasp Diachasma alloeum, an Emerging Model for Ecological Speciation and Transitions to Asexual Reproduction

Wed, 25 Sep 2019 00:00:00 GMT

Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae), and a developing model for understanding how ecological speciation can “cascade” across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated ∼400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.

Genetics of Adaptation of the Ascomycetous Fungus Podospora anserina to Submerged Cultivation

Sat, 14 Sep 2019 00:00:00 GMT

Podospora anserina is a model ascomycetous fungus which shows pronounced phenotypic senescence when grown on solid medium but possesses unlimited lifespan under submerged cultivation. In order to study the genetic aspects of adaptation of P. anserina to submerged cultivation, we initiated a long-term evolution experiment. In the course of the first 4 years of the experiment, 125 single-nucleotide substitutions and 23 short indels were fixed in eight independently evolving populations. Six proteins that affect fungal growth and development evolved in more than one population; in particular, in the G-protein alpha subunit FadA, new alleles fixed in seven out of eight experimental populations, and these fixations affected just four amino acid sites, which is an unprecedented level of parallelism in experimental evolution. Parallel evolution at the level of genes and pathways, an excess of nonsense and missense substitutions, and an elevated conservation of proteins and their sites where the changes occurred suggest that many of the observed fixations were adaptive and driven by positive selection.

Large-Scale Molecular Evolutionary Analysis Uncovers a Variety of Polynucleotide Kinase Clp1 Family Proteins in the Three Domains of Life

Thu, 12 Sep 2019 00:00:00 GMT

Clp1, a polyribonucleotide 5′-hydroxyl kinase in eukaryotes, is involved in pretRNA splicing and mRNA 3′-end formation. Enzymes similar in amino acid sequence to Clp1, Nol9, and Grc3, are present in some eukaryotes and are involved in prerRNA processing. However, our knowledge of how these Clp1 family proteins evolved and diversified is limited. We conducted a large-scale molecular evolutionary analysis of the Clp1 family proteins in all living organisms for which protein sequences are available in public databases. The phylogenetic distribution and frequencies of the Clp1 family proteins were investigated in complete genomes of Bacteria, Archaea and Eukarya. In total, 3,557 Clp1 family proteins were detected in the three domains of life, Bacteria, Archaea, and Eukarya. Many were from Archaea and Eukarya, but a few were found in restricted, phylogenetically diverse bacterial species. The domain structures of the Clp1 family proteins also differed among the three domains of life. Although the proteins were, on average, 555 amino acids long (range, 196–2,728), 122 large proteins with >1,000 amino acids were detected in eukaryotes. These novel proteins contain the conserved Clp1 polynucleotide kinase domain and various other functional domains. Of these proteins, >80% were from Fungi or Protostomia. The polyribonucleotide kinase activity of Thermus scotoductus Clp1 (Ts-Clp1) was characterized experimentally. Ts-Clp1 preferentially phosphorylates single-stranded RNA oligonucleotides (Km value for ATP, 2.5 µM), or single-stranded DNA at higher enzyme concentrations. We propose a comprehensive assessment of the diversification of the Clp1 family proteins and the molecular evolution of their functional domains.

Molecular Evolution in Small Steps under Prevailing Negative Selection: A Nearly Universal Rule of Codon Substitution

Mon, 09 Sep 2019 00:00:00 GMT

The widely accepted view that evolution proceeds in small steps is based on two premises: 1) negative selection acts strongly against large differences and 2) positive selection favors small-step changes. The two premises are not biologically connected and should be evaluated separately. We now extend a previous approach to studying codon evolution in the entire genome. Codon substitution rate is a function of the physicochemical distance between amino acids (AAs), equated with the step size of evolution. Between nine pairs of closely related species of plants, invertebrates, and vertebrates, the evolutionary rate is strongly and negatively correlated with a set of AA distances (ΔU, scaled to [0, 1]). ΔU, a composite measure of evolutionary rates across diverse taxa, is influenced by almost all of the 48 physicochemical properties used here. The new analyses reveal a crucial trend hidden from previous studies: ΔU is strongly correlated with the evolutionary rate (R2 > 0.8) only when the genes are predominantly under negative selection. Because most genes in most taxa are strongly constrained by negative selection, ΔU has indeed appeared to be a nearly universal measure of codon evolution. In conclusion, molecular evolution at the codon level generally takes small steps due to the prevailing negative selection. Whether positive selection may, or may not, follow the small-step rule is addressed in a companion study.

Sea Turtle Population Genomic Discovery: Global and Locus-Specific Signatures of Polymorphism, Selection, and Adaptive Potential

Wed, 04 Sep 2019 00:00:00 GMT

In the era of genomics, single-nucleotide polymorphisms (SNPs) have become a preferred molecular marker to study signatures of selection and population structure and to enable improved population monitoring and conservation of vulnerable populations. We apply a SNP calling pipeline to assess population differentiation, visualize linkage disequilibrium, and identify loci with sex-specific genotypes of 45 loggerhead sea turtles (Caretta caretta) sampled from the southeastern coast of the United States, including 42 individuals experimentally confirmed for gonadal sex. By performing reference-based SNP calling in independent runs of Stacks, 3,901–6,998 SNPs and up to 30 potentially sex-specific genotypes were identified. Up to 68 pairs of loci were found to be in complete linkage disequilibrium, potentially indicating regions of natural selection and adaptive evolution. This study provides a valuable SNP diagnostic workflow and a large body of new biomarkers for guiding targeted studies of sea turtle genome evolution and for managing legally protected nonmodel iconic species that have high economic and ecological importance but limited genomic resources.

Plastome Reduction in the Only Parasitic Gymnosperm Parasitaxus Is Due to Losses of Photosynthesis but Not Housekeeping Genes and Apparently Involves the Secondary Gain of a Large Inverted Repeat

Tue, 27 Aug 2019 00:00:00 GMT

Plastid genomes (plastomes) of parasitic plants undergo dramatic reductions as the need for photosynthesis relaxes. Here, we report the plastome of the only known heterotrophic gymnosperm Parasitaxus usta (Podocarpaceae). With 68 unique genes, of which 33 encode proteins, 31 tRNAs, and four rRNAs in a plastome of 85.3-kb length, Parasitaxus has both the smallest and the functionally least capable plastid genome of gymnosperms. Although the heterotroph retains chlorophyll, all genes for photosynthesis are physically or functionally lost, making photosynthetic energy gain impossible. The pseudogenization of the three plastome-encoded light-independent chlorophyll biosynthesis genes chlB, chlL, and chlN implies that Parasitaxus relies on either only the light-dependent chlorophyll biosynthesis pathway or another regulation system. Nesting within a group of gymnosperms known for the absence of the large inverted repeat regions (IRs), another unusual feature of the Parasitaxus plastome is the existence of a 9,256-bp long IR. Its short length and a gene composition that completely differs from those of IR-containing gymnosperms together suggest a regain of this critical, plastome structure-stabilizing feature. In sum, our findings highlight the particular path of lifestyle-associated reductive plastome evolution, where structural features might provide additional cues of a continued selection for plastome maintenance.

Current and Promising Approaches to Identify Horizontal Gene Transfer Events in Metagenomes

Mon, 26 Aug 2019 00:00:00 GMT

High-throughput shotgun metagenomics sequencing has enabled the profiling of myriad natural communities. These data are commonly used to identify gene families and pathways that were potentially gained or lost in an environment and which may be involved in microbial adaptation. Despite the widespread interest in these events, there are no established best practices for identifying gene gain and loss in metagenomics data. Horizontal gene transfer (HGT) represents several mechanisms of gene gain that are especially of interest in clinical microbiology due to the rapid spread of antibiotic resistance genes in natural communities. Several additional mechanisms of gene gain and loss, including gene duplication, gene loss-of-function events, and de novo gene birth are also important to consider in the context of metagenomes but have been less studied. This review is largely focused on detecting HGT in prokaryotic metagenomes, but methods for detecting these other mechanisms are first discussed. For this article to be self-contained, we provide a general background on HGT and the different possible signatures of this process. Lastly, we discuss how improved assembly of genomes from metagenomes would be the most straight-forward approach for improving the inference of gene gain and loss events. Several recent technological advances could help improve metagenome assemblies: long-read sequencing, determining the physical proximity of contigs, optical mapping of short sequences along chromosomes, and single-cell metagenomics. The benefits and limitations of these advances are discussed and open questions in this area are highlighted.

Expressed Vomeronasal Type-1 Receptors (V1rs) in Bats Uncover Conserved Sequences Underlying Social Chemical Signaling

Mon, 19 Aug 2019 00:00:00 GMT

In mammals, social and reproductive behaviors are mediated by chemical cues encoded by hyperdiverse families of receptors expressed in the vomeronasal organ. Between species, the number of intact receptors can vary by orders of magnitude. However, the evolutionary processes behind variation in receptor number, and its link to fitness-related behaviors are not well understood. From vomeronasal transcriptomes, we discovered the first evidence of intact vomeronasal type-1 receptor (V1r) genes in bats, and we tested whether putatively functional bat receptors were orthologous to those of related taxa, or whether bats have evolved novel receptors. Instead of lineage-specific duplications, we found that bat V1rs show high levels of orthology to those of their relatives, and receptors are under comparative levels of purifying selection as non-bats. Despite widespread vomeronasal organ loss in bats, V1r copies have been retained for >65 million years. The highly conserved nature of bat V1rs challenges our current understanding of mammalian V1r function and suggests roles other than conspecific recognition or mating initiation in social behavior.

Evidence of Extensive Intraspecific Noncoding Reshuffling in a 169-kb Mitochondrial Genome of a Basidiomycetous Fungus

Fri, 16 Aug 2019 00:00:00 GMT

Comparative genomics of fungal mitochondrial genomes (mitogenomes) have revealed a remarkable pattern of rearrangement between and within major phyla owing to horizontal gene transfer and recombination. The role of recombination was exemplified at a finer evolutionary time scale in basidiomycetes group of fungi as they display a diversity of mitochondrial DNA inheritance patterns. Here, we assembled mitogenomes of six species from the Hymenochaetales order of basidiomycetes and examined 59 mitogenomes from 2 genetic lineages of Phellinus noxius. Gene order is largely collinear, while intergene regions are major determinants of mitogenome size variation. Substantial sequence divergence was found in shared introns consistent with high horizontal gene transfer frequency observed in yeasts, but we also identified a rare case where an intron was retained in five species since speciation. In contrast to the hyperdiversity observed in nuclear genomes of Phellinus noxius, mitogenomes’ intraspecific polymorphisms at protein-coding sequences are extremely low. Phylogeny network based on introns revealed turnover as well as exchange of introns between two lineages. Strikingly, some strains harbor a mosaic origin of introns from both lineages. Analysis of intergenic sequence indicated substantial differences between and within lineages, and an expansion may be ongoing as a result of exchange between distal intergenes. These findings suggest that the evolution in mitochondrial DNAs is usually lineage specific but chimeric mitotypes are frequently observed, thus capturing the possible evolutionary processes shaping mitogenomes in a basidiomycete. The large mitogenome sizes reported in various basidiomycetes appear to be a result of interspecific reshuffling of intergenes.

Nephromyces Represents a Diverse and Novel Lineage of the Apicomplexa That Has Retained Apicoplasts

Mon, 22 Jul 2019 00:00:00 GMT

A most interesting exception within the parasitic Apicomplexa is Nephromyces, an extracellular, probably mutualistic, endosymbiont found living inside molgulid ascidian tunicates (i.e., sea squirts). Even though Nephromyces is now known to be an apicomplexan, many other questions about its nature remain unanswered. To gain further insights into the biology and evolutionary history of this unusual apicomplexan, we aimed to 1) find the precise phylogenetic position of Nephromyces within the Apicomplexa, 2) search for the apicoplast genome of Nephromyces, and 3) infer the major metabolic pathways in the apicoplast of Nephromyces. To do this, we sequenced a metagenome and a metatranscriptome from the molgulid renal sac, the specialized habitat where Nephromyces thrives. Our phylogenetic analyses of conserved nucleus-encoded genes robustly suggest that Nephromyces is a novel lineage sister to the Hematozoa, which comprises both the Haemosporidia (e.g., Plasmodium) and the Piroplasmida (e.g., Babesia and Theileria). Furthermore, a survey of the renal sac metagenome revealed 13 small contigs that closely resemble the genomes of the nonphotosynthetic reduced plastids, or apicoplasts, of other apicomplexans. We show that these apicoplast genomes correspond to a diverse set of most closely related but genetically divergent Nephromyces lineages that co-inhabit a single tunicate host. In addition, the apicoplast of Nephromyces appears to have retained all biosynthetic pathways inferred to have been ancestral to parasitic apicomplexans. Our results shed light on the evolutionary history of the only probably mutualistic apicomplexan known, Nephromyces, and provide context for a better understanding of its life style and intricate symbiosis.