Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria

Paula B Matheus Carnevali,Karthik Anantharaman,Frederik Schulz,Patrick M Shih,Tanja Woyke,Matthew R Olm,Jillian F Banfield,David Burstein,Itai Sharon,Yuki Amano,Joanne M Santini,Ramunas Stepanauskas,Cindy J Castelle,Brian C Thomas,Eric D Becraft,Rose S Kantor

doi:10.1038/s41467-018-08246-y

Abstract

The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria. Close phylogenetic neighbors to Cyanobacteria, such as Margulisbacteria (RBX-1 and ZB3), Saganbacteria (WOR-1), Melainabacteria and Sericytochromatia, may constrain the metabolic platform in which aerobic respiration arose. Here, we analyze genomic sequences and predict that sediment-associated Margulisbacteria have a fermentation-based metabolism featuring a variety of hydrogenases, a streamlined nitrogenase, and electron bifurcating complexes involved in cycling of reducing equivalents. The genomes of ocean-associated Margulisbacteria encode an electron transport chain that may support aerobic growth. Some Saganbacteria genomes encode various hydrogenases, and others may be able to use O2 under certain conditions via a putative novel type of heme copper O2 reductase. Similarly, Melainabacteria have diverse energy metabolisms and are capable of fermentation and aerobic or anaerobic respiration. The ancestor of all these groups may have been an anaerobe in which fermentation and H2 metabolism were central metabolic features. The ability to use O2 as a terminal electron acceptor must have been subsequently acquired by these lineages.

Highlights

The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria
We investigate genomes of Margulisbacteria (RBX-1) and Saganbacteria (WOR-1), lineages related to both Melainabacteria and Sericytochromatia, and identify common mechanisms for energy conservation that may have been present in their common ancestor with Cyanobacteria
We found that H2 metabolism is a common feature of the modern groups that cannot respire aerobically, and suggest that hydrogenases may have been central to the lifestyles of the ancestors of Cyanobacteria, Melainabacteria, Sericytochromatia, Margulisbacteria, and Saganbacteria

Summary

Introduction

The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria. We investigate genomes of Margulisbacteria (RBX-1) and Saganbacteria (WOR-1), lineages related to both Melainabacteria and Sericytochromatia, and identify common mechanisms for energy conservation that may have been present in their common ancestor with Cyanobacteria. Marinamargulisbacteria was first observed in a clone library of SSU rRNA genes from Zodletone spring (Oklahoma) and identified as candidate division ZB311 We leverage these genomes, and new genomes for Margulisbacteria and members of the Melainabacteria to predict how organisms from these lineages conserve energy in the form of ATP, identify their potential strategies for reoxidation of reducing equivalents, and propose the interconnectedness between H2 and O2 metabolism. We found that H2 metabolism is a common feature of the modern groups that cannot respire aerobically, and suggest that hydrogenases may have been central to the lifestyles of the ancestors of Cyanobacteria, Melainabacteria, Sericytochromatia, Margulisbacteria, and Saganbacteria

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Results

Conclusion