Pangenome Evidence for Extensive Interdomain Horizontal Transfer Affecting Lineage Core and Shell Genes in Uncultured Planktonic Thaumarchaeota and Euryarchaeota

Philippe Deschamps,Francisco Rodriguez-Valera,Purificación López-García,David Moreira,Yvan Zivanovic

doi:10.1093/gbe/evu127

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.

Highlights

More than 1 decade ago, the exploration of microbial environmental diversity with molecular tools led to the discovery of several archaeal lineages in the oceanic water column
Because Thaumarchaeota and GII/III-Euryarchaeota seem to have a single copy of rRNA genes (Moreira et al 2004), the number of archaeal genomes sequenced could be estimated at, respectively, 14 and 9, based on the number of rRNA gene copies identified
A principal component analysis (PCA) of tetranucleotide frequencies showed a clear separation of Thaumarchaeota and Euryarchaeota fosmids

Summary

Introduction

More than 1 decade ago, the exploration of microbial environmental diversity with molecular tools led to the discovery of several archaeal lineages in the oceanic water column. Group I archaea branched at the base of the classical Crenarchaeota, one archaeal lineage so far composed exclusively of hyperthermophilic members, and raised increasing interest in subsequent years. It proved to be diverse and widespread in oceans, where it was abundant at high depth (Karner et al 2001; DeLong et al 2006; Martin-Cuadrado et al 2008), and in freshwater and soils (Schleper et al 2005; Leininger et al 2006).

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