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Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota.

ABSTRACT: Horizontal gene transfer (HGT) is an important force in evolution, which may lead, among other things, to the adaptation to new environments by the import of new metabolic functions. Recent studies based on phylogenetic analyses of a few genome fragments containing archaeal 16S rRNA genes and fosmid-end sequences from deep-sea metagenomic libraries have suggested that marine planktonic archaea could be affected by high HGT frequency. Likewise, a composite genome of an uncultured marine euryarchaeote showed high levels of gene sequence similarity to bacterial genes. In this work, we ask whether HGT is frequent and widespread in genomes of these marine archaea, and whether HGT is an ancient and/or recurrent phenomenon. To answer these questions, we sequenced 997 fosmid archaeal clones from metagenomic libraries of deep-Mediterranean waters (1,000 and 3,000 m depth) and built comprehensive pangenomes for planktonic Thaumarchaeota (Group I archaea) and Euryarchaeota belonging to the uncultured Groups II and III Euryarchaeota (GII/III-Euryarchaeota). Comparison with available reference genomes of Thaumarchaeota and a composite marine surface euryarchaeote genome allowed us to define sets of core, lineage-specific core, and shell gene ortholog clusters for the two archaeal lineages. Molecular phylogenetic analyses of all gene clusters showed that 23.9% of marine Thaumarchaeota genes and 29.7% of GII/III-Euryarchaeota genes had been horizontally acquired from bacteria. HGT is not only extensive and directional but also ongoing, with high HGT levels in lineage-specific core (ancient transfers) and shell (recent transfers) genes. Many of the acquired genes are related to metabolism and membrane biogenesis, suggesting an adaptive value for life in cold, oligotrophic oceans. We hypothesize that the acquisition of an important amount of foreign genes by the ancestors of these archaeal groups significantly contributed to their divergence and ecological success.

SUBMITTER: Deschamps P

PROVIDER: S-EPMC4122925 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota.

Deschamps Philippe P Zivanovic Yvan Y Moreira David D Rodriguez-Valera Francisco F López-García Purificación P

Genome biology and evolution 20140612 7

Horizontal gene transfer (HGT) is an important force in evolution, which may lead, among other things, to the adaptation to new environments by the import of new metabolic functions. Recent studies based on phylogenetic analyses of a few genome fragments containing archaeal 16S rRNA genes and fosmid-end sequences from deep-sea metagenomic libraries have suggested that marine planktonic archaea could be affected by high HGT frequency. Likewise, a composite genome of an uncultured marine euryarcha ...[more]

PMID: 24923324

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Project description:The extent of horizontal gene transfer (HGT) among marine pelagic prokaryotes and the role that HGT may have played in their adaptation to this particular environment remain open questions. This is partly due to the paucity of cultured species and genomic information for many widespread groups of marine bacteria and archaea. Molecular studies have revealed a large diversity and relative abundance of marine planktonic archaea, in particular of Thaumarchaeota (also known as group I Crenarchaeota) and Euryarchaeota of groups II and III, but only one species (the thaumarchaeote Candidatus Nitrosopumilus maritimus) has been isolated in pure culture so far. Therefore, metagenomics remains the most powerful approach to study these environmental groups. To investigate the impact of HGT in marine archaea, we carried out detailed phylogenetic analyses of all open reading frames of 21 archaeal 16S rRNA gene-containing fosmids and, to extend our analysis to other genomic regions, also of fosmid-end sequences of 12 774 fosmids from three different deep-sea locations (South Atlantic and Adriatic Sea at 1000 m depth, and Ionian Sea at 3000 m depth). We found high HGT rates in both marine planktonic Thaumarchaeota and Euryarchaeota, with remarkable converging values estimated from complete-fosmid and fosmid-end sequence analysis (25 and 21% of the genes, respectively). Most HGTs came from bacterial donors (mainly from Proteobacteria, Firmicutes and Chloroflexi) but also from other archaea and eukaryotes. Phylogenetic analyses showed that in most cases HGTs are shared by several representatives of the studied groups, implying that they are ancient and have been conserved over relatively long evolutionary periods. This, together with the functions carried out by these acquired genes (mostly related to energy metabolism and transport of metabolites across membranes), suggests that HGT has played an important role in the adaptation of these archaea to the cold and nutrient-depleted deep marine environment.

Project description:The ubiquitous and abundant distribution of ammonia-oxidizing Thaumarchaeota in marine environments is now well documented, and their crucial role in the global nitrogen cycle has been highlighted. However, the potential contribution of Thaumarchaeota in the carbon cycle remains poorly understood. Here we present for the first time a seasonal investigation on the shelf region (bathymetry≤200 m) of the East China Sea (ECS) involving analysis of both thaumarchaeal 16S rRNA and autotrophy-related genes (acetyl-CoA carboxylase gene, accA). Quantitative PCR results clearly showed a higher abundance of thaumarchaeal 16S and accA genes in late-autumn (November) than summer (August), whereas the diversity and community structure of autotrophic Thaumarchaeota showed no statistically significant difference between different seasons as revealed by thaumarchaeal accA gene clone libraries. Phylogenetic analysis indicated that shallow ecotypes dominated the autotrophic Thaumarchaeota in the ECS shelf (86.3% of total sequences), while a novel non-marine thaumarchaeal accA lineage was identified in the Changjiang estuary in summer (when freshwater plumes become larger) but not in autumn, implying that Changjiang freshwater discharge played a certain role in transporting terrestrial microorganisms to the ECS. Multivariate statistical analysis indicated that the biogeography of the autotrophic Thaumarchaeota in the shelf water of the ECS was influenced by complex hydrographic conditions. However, an in silico comparative analysis suggested that the diversity and abundance of the autotrophic Thaumarchaeota might be biased by the 'universal' thaumarchaeal accA gene primers Cren529F/Cren981R since this primer set is likely to miss some members within particular phylogenetic groups. Collectively, this study improved our understanding of the biogeographic patterns of the autotrophic Thaumarchaeota in temperate coastal waters, and suggested that new accA primers with improved coverage and sensitivity across phylogenetic groups are needed to gain a more thorough understanding of the role of the autotrophic Thaumarchaeota in the global carbon cycle.

Dataset Information

Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota.

Publications

Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota.

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