Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

Sheridan, Paul O.; Raguideau, Sébastien; Quince, Christopher; Holden, Jennifer; Zhang, Lihong; Williams, Tom A.; Gubry‐Rangin, Cécile

doi:10.1038/s41467-020-19132-x

Cited by 68 publications

(119 citation statements)

References 92 publications

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“…Thus, modules enriched in specific lineages were probably acquired via lateral transfer after habitat transition, suggesting that proteome remodeling has been continuous in CPR over evolutionary time. As such, the processes shaping CPR lineage evolution share both similarities and differences with those predicted for other microbes, including Haloarchaeota (94) and ammonia-oxidizing lineages of Thaumarchaeota (88, 95), where both large lateral transfer events and gradual patterns of gene loss, gain, and duplication worked together to shape major habitat transitions.…”

Section: Discussionmentioning

confidence: 89%

“…To do so, we first inferred unrooted, maximum-likelihood phylogenies for the sequences in each protein family that was differentially distributed, then compared these phylogenies to the previously reconstructed species tree (Materials and Methods). For each family, the likelihood of transfer and loss events on each branch of the species tree were then estimated using a probabilistic framework that takes into consideration genome incompleteness, variable rates of transfer and loss, and uncertainty in gene tree reconstruction (88, 89). The results of this analysis reveal relatively few instances of originations, defined as lateral transfer from outside the three lineages of CPR or de novo evolution (‘originations’, Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To examine the evolutionary processes shaping the differentially-distributed protein families, we next subjected each family to an automated gene-species tree reconciliation workflow adapted from (88). Briefly, for each family, truncated sequences (defined as those with lengths less than 2 standard deviations from the family mean) were removed and the remaining sequences aligned with MAFFT ( --retree 2).…”

Section: Methodsmentioning

confidence: 99%

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Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

Jaffe¹,

Keren³

et al. 2021

Preprint

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Bacteria from the Candidate Phyla Radiation (CPR) are small, likely episymbiotic organisms found across Earth's ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions amongst these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By combining phylogeny and habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Using computational co-occurrence analyses based on hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that Saccharibacteria from animal-associated microbiomes have, on average, smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative bacteriorhodopsin. For protein families that exhibited the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss that occurred over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events, but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa, and were reinforced by acquisition and loss of some capacities.

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Section: Discussionmentioning

confidence: 89%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

Jaffe¹,

Keren³

et al. 2021

Preprint

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“…HGT can foster the acquisition of new functions while duplications relate to a higher gene dosage (47). However, phylogenomic analysis of other lineages such as Nitrososphaerales (Thermoproteota) indicate a predominant role of gene duplications over HGT (48). These examples highlight how HGT and duplications aid microorganisms into adaptation to their niches.…”

Section: Genetic Processes That Shape Genome Sizementioning

confidence: 99%

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Rodríguez-Gijón

Nuy

Mehrshad

et al. 2021

Preprint

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Our view of genome size distribution in Bacteria and Archaea has remained skewed as the data used to paint its picture has been dominated by genomes of microorganisms that can be cultivated under laboratory settings. However, the continuous effort to catalogue the genetic make-up of Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides a unique opportunity to revise our perspective on genome size distribution. Genome size is largely a function of the expansion and contraction, by gain or loss of DNA elements. While genome expansion provides microorganisms the capability to acquire a wide repertoire of ecological functions, genome reduction increases the fitness of the microorganisms to very specific niches. Capitalizing on a recently released large catalog of tens of thousands of metagenome-assembled genomes, we here provide a comprehensive overview of genome size distributions, suggesting that the known phylogenetic diversity of environmental microorganisms possess significantly smaller genomes (aquatic bacteria average 3.1 Mb, host-associated bacterial genomes average 3.0 Mb, and terrestrial bacteria average 3.8 Mb) than the collection of laboratory isolated microorganisms (average 4.4 Mb). Moreover, the variation in genome sizes across different types of environments reflects the different ecological and evolutionary strategies used by microorganisms to thrive in their native environment. Finally, the fact that genome sizes in Bacteria and Archaea remain relatively small might be a reflection of the constraints imposed by selection and an overall dominance of gene loss as a survival strategy.

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“…Expansion or contraction of gene families has been cited as a general mechanism for such adaptations [1,2]. Expansions arise mainly from gene duplication and, in some cases, from acquisition via horizontal gene transfer, whereas gene loss can happen by accumulation of loss-offunction mutations through genetic drift [3,4,5]. Fundamentally, both of these processes are driven by adaptive evolution, whereby beneficial mutations are selected for and deleterious removed from the gene pool, ultimately leading to phenotypic diversification [6].…”

Section: Introductionmentioning

confidence: 99%

Predicting lifestyle and host from positive selection data and genome properties in oomycetes

Gómez-Pérez

Kemen

2021

Preprint

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BackgroundHost and niche shifts are a source of genomic and phenotypic diversification as evidenced in parasitism. Most characteristic is core metabolism reduction as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversification. However, selective pressures acting on the genome of such organisms are not fully understood.ResultsHere, we developed a comparative genomic approach to study underlying adaptive trends in oomycetes, a eukaryote phylum with a broad range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes inhabiting similar niches. We find that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaption in oomycetes.DiscussionGiven the high correlation of lifestyle to genome properties in our oomycete dataset and the convergent evolution of fungal and oomycete genomes, we have developed a model that predicts plant pathogen lifestyles with high accuracy. Understanding how genomes and selective pressures correlate with lifestyle may be crucial to identify new emerging diseases and pandemic threats.

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Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

Cited by 68 publications

References 92 publications

Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Predicting lifestyle and host from positive selection data and genome properties in oomycetes

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