(Meta)Genomic Analysis Reveals Diverse Energy Conservation Strategies Employed by Globally Distributed Gemmatimonadota

Abstract

ABSTRACT Gemmatimonadota is a phylum-level lineage distributed widely but rarely reported. Only six representatives of Gemmatimonadota have so far been isolated and cultured in laboratory. The physiology, ecology, and evolutionary history of this phylum remain unknown. The 16S rRNA gene survey of our salt lake and deep-sea sediments, and Earth Microbiome Project (EMP) samples, reveals that Gemmatimonadota exist in diverse environments globally. In this study, we retrieved 17 metagenome-assembled genomes (MAGs) from salt lake sediments (12 MAGs) and deep-sea sediments (5 MAGs). Analysis of these MAGs and the nonredundant MAGs or genomes from public databases reveals Gemmatimonadota can degrade various complex organic substrates, and mainly employ heterotrophic pathways (e.g., glycolysis and tricarboxylic acid [TCA] cycle) for growth via aerobic respiration. And the processes of sufficient energy being stored in glucose through gluconeogenesis, followed by the synthesis of more complex compounds, are prevalent in Gemmatimonadota. A highly expandable pangenome for Gemmatimonadota has been observed, which presumably results from their adaptation to thriving in diverse environments. The enrichment of the Na+/H+ antiporter in the SG8-23 order represents their adaptation to salty habitats. Notably, we identified a novel lineage of the SG8-23 order, which is potentially anoxygenic phototrophic. This lineage is not closely related to the phototrophs in the order of Gemmatimonadales. The two orders differ distinctly in the gene organization and phylogenetic relationship of their photosynthesis gene clusters, indicating photosystems in Gemmatimonadota have evolved in two independent routes. IMPORTANCE The phylum Gemmatimonadota is widely distributed in various environments. However, their physiology, ecology and evolutionary history remain unknown, primary due to the limited cultured isolates and available genomes. We were intrigued to find out how widespread this phylum is, and how it can thrive under diverse conditions. Our results here expand the knowledge of the genetic and metabolic diversity of Gemmatimonadota, and shed light on the diverse energy conservation strategies (i.e., oxidative phosphorylation, substrate phosphorylation, and photosynthetic phosphorylation) responsible for their global distribution. Moreover, gene organization and phylogenetic analysis of photosynthesis gene clusters in Gemmatimonadota provide a valuable insight into the evolutionary history of photosynthesis.

Keywords

• metagenome
• Gemmatimonadota
• anoxygenic phototrophs
• photosynthesis gene cluster
• physiology
• phylogeny