Genomic insight of sulfate reducing bacterial genus Desulfofaba reveals their metabolic versatility in biogeochemical cycling

Abstract

Background: Sulfate-reducing bacteria (SRB) drive the ocean sulfur and carbon cycling. They constitute a diverse phylogenetic and physiological group and are widely distributed in anoxic marine environments. From a physiological viewpoint, SRB's can be categorized as complete or incomplete oxidizers, meaning that they either oxidize their carbon substrate completely to CO₂ or to a stoichiometric mix of CO₂ and acetate. Members of Desulfofabaceae family are incomplete oxidizers, and within that family, Desulfofaba is the only genus with three isolates that are classified into three species. Previous physiological experiments revealed their capability of respiring oxygen.

Results: Here, we sequenced the genomes of three isolates in Desulfofaba genus and reported on a genomic comparison of the three species to reveal their metabolic potentials. Based on their genomic contents, they all could oxidize propionate to acetate and CO₂. We confirmed their phylogenetic position as incomplete oxidizers based on dissimilatory sulfate reductase (DsrAB) phylogeny. We found the complete pathway for dissimilatory sulfate reduction, but also different key genes for nitrogen cycling, including nitrogen fixation, assimilatory nitrate/nitrite reduction, and hydroxylamine reduction to nitrous oxide. Their genomes also contain genes that allow them to cope with oxygen and oxidative stress. They have genes that encode for diverse central metabolisms for utilizing different substrates with the potential for more strains to be isolated in the future, yet their distribution is limited.

Conclusions: Results based on marker gene search and curated metagenome assembled genomes search suggest a limited environmental distribution of this genus. Our results reveal a large metabolic versatility within the Desulfofaba genus which establishes their importance in biogeochemical cycling of carbon in their respective habitats, as well as in the support of the entire microbial community through releasing easily degraded organic matters.

Keywords: Desulfofaba; Genome; Incomplete sulfate reducer; Nitrogen; Oxygen; Sulfur.

Fig. 1

A maximum likelihood phylogenetic tree of 22 genomes including the 3 Desulfofaba genomes. The phylogeny is based on 37 concatenated ribosomal protein encoding genes identified using PhyloSift. Desulfofaba genomes formed a monophyletic group which is distinct from other families in the order Desulfobacterales. Acidobacteria were set as the outgroup

Fig. 2

Overview of the metabolic potential of the Desulfofaba genus based on the annotated genomes. Desulfofaba genomes have genes encoding for diverse central metabolic pathways, including glycolysis, the pentose phosphate pathway (PPP), the Wood-Ljungdahl pathway (WLP), the TCA cycle, and the reductive glycine pathway. Desulfofaba genomes have genes involved in nitrogen, sulfur, hydrogen, selenium, and arsenic cycling. Different types of cytochrome oxidases genes were annotated in Desulfofaba genomes

Fig. 3

A maximum likelihood phylogenetic tree of genes encoding for alpha and beta subunits of dissimilatory sulfite reductase (DsrAB). DsrAB in Desulfofaba genomes belong to reductive-type and are closely related to sequences in known incomplete oxidizer genomes

Fig. 4

Shared protein contents among three Desulfofaba genomes based on two different algorithms: a bidirectional best-hits (BDBH) and b orthoMCL algorithm (OMCL). Over 1500 proteins were shared between the three species, and over 1/3 of protein sequences in each genome were species-specific