Abstract

BackgroundA unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities. However, the distribution of metabolic traits across the CPR and the evolutionary processes underlying them are incompletely resolved.ResultsHere, we selected ~ 1000 genomes of CPR bacteria from diverse environments to construct a robust internal phylogeny that was consistent across two unlinked marker sets. Mapping of glycolysis, the pentose phosphate pathway, and pyruvate metabolism onto the tree showed that some components of these pathways are sparsely distributed and that similarity between metabolic platforms is only partially predicted by phylogenetic relationships. To evaluate the extent to which gene loss and lateral gene transfer have shaped trait distribution, we analyzed the patchiness of gene presence in a phylogenetic context, examined the phylogenetic depth of clades with shared traits, and compared the reference tree topology with those of specific metabolic proteins. While the central glycolytic pathway in CPR is widely conserved and has likely been shaped primarily by vertical transmission, there is evidence for both gene loss and transfer especially in steps that convert glucose into fructose 1,6-bisphosphate and glycerate 3P into pyruvate. Additionally, the distribution of Group 3 and Group 4-related NiFe hydrogenases is patchy and suggests multiple events of ancient gene transfer.ConclusionsWe infer that patterns of gene gain and loss in CPR, including acquisition of accessory traits in independent transfer events, could have been driven by shifts in host-derived resources and led to sparse but varied genetic inventories.

Highlights

  • A unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities

  • Phylogenies based on these two marker sets were generally congruent for deep relationships within the CPR, with both trees supporting the distinction of CPR from the bacterial outgroup and the monophyly of the Microgenomates and Parcubacteria superphyla, respectively (Fig. 1a; Additional file 2, Fig. S2)

  • Some clades were supported by the absence of particular ribosomal proteins—the Microgenomates, along with the Dojkabacteria and Katanobacteria, lacked ribosomal protein L9, while a subset of Parcubacteria lacked the ribosomal protein L1, as observed previously [1]

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Summary

Introduction

A unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities. The distribution of metabolic traits across the CPR and the evolutionary processes underlying them are incompletely resolved. Genomes recovered from poorly represented or novel groups have helped greatly to elucidate the evolutionary processes contributing both to broad bacterial and archaeal diversity and to the distribution of metabolic capacities over various lineages [5,6,7]. The Candidate Phyla Radiation is a large group of bacterial lineages that lack pure isolate cultures and have been primarily defined through genome-resolved metagenomics [1, 8]. CPR bacteria generally have relatively small genome and cell sizes, have extremely reduced genomic repertoires, and often lack the capacity to synthesize lipids, amino acids, and nucleotides [1, 8, 12]. The CPR may have diverged early from other bacteria and subsequently diversified over long periods of time, or they

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