Diversity and metabolism of Woeseiales bacteria, global members of marine sediment communities

Pierre Offre,Antje Boetius,Katrin Knittel,Katy Hoffmann,Josephine Z Rapp,Rafael Laso-Pérez,Christina Bienhold,Pier Luigi Buttigieg

doi:10.1038/s41396-020-0588-4

Abstract

Surveys of 16S rRNA gene sequences derived from marine sediments have indicated that a widely distributed group of Gammaproteobacteria, named “JTB255-Marine Benthic Group” (now the candidate order Woeseiales), accounts for 1–22% of the retrieved sequences. Despite their ubiquity in seafloor communities, little is known about their distribution and specific ecological niches in the deep sea, which constitutes the largest biome globally. Here, we characterized the phylogeny, environmental distribution patterns, abundance, and metabolic potential of Woeseiales bacteria with a focus on representatives from the deep sea. From a phylogenetic analysis of publicly available 16S rRNA gene sequences (≥1400 bp, n = 994), we identified lineages of Woeseiales with greater prevalence in the deep sea than in coastal environments, a pattern corroborated by the distribution of 16S oligotypes recovered from 28 globally distributed sediment samples. Cell counts revealed that Woeseiales bacteria accounted for 5 ± 2% of all microbial cells in deep-sea surface sediments at 23 globally distributed sites. Comparative analyses of a genome, metagenome bins, and single-cell genomes suggested that members of the corresponding clades are likely to grow on proteinaceous matter, potentially derived from detrital cell membranes, cell walls, and other organic remnants in marine sediments.

Highlights

Marine sediments cover ~70% of Earth’s surface, hosting a huge diversity of bacterial populations that gain energy and nutrients from the remineralization of sedimented organic matter [1, 2]
We investigated the environmental distribution of 16S rRNA gene sequences of Woeseiales bacteria in order to evaluate whether distinct taxa within Woeseiales associate with different environments, with a main focus on deep-sea and coastal environments
We investigated the phylogenetic placement of 171 phylotypes, which cover the diversity of all 16S rRNA gene clone sequences (≥1400 bp) assigned to JTB255-MBG in SILVA 128

Summary

Introduction

Marine sediments cover ~70% of Earth’s surface, hosting a huge diversity of bacterial populations that gain energy and nutrients from the remineralization of sedimented organic matter [1, 2]. The identity and relative contributions of the major groups of microorganisms involved in the degradation of sedimentary biomacromolecules remain unknown This is further emphasized by the high degree of spatial heterogeneity of the seafloor in microbial community composition and organic matter deposition, recycling, and burial in different regions of the seafloor, e.g., between shallow coastal sediments and deep oceanic sediments [2, 3]. Recent surveys of 16S rRNA gene sequences have revealed that the largely uncultivated group of Gammaproteobacteria formerly known as “JTB255-Marine Benthic Group” (abbreviated JTB255-MBG) is globally distributed in both coastal and deep-sea sediments [4,5,6,7] In these studies, members of this group account for 1–22% of the sequences retrieved. The main hypotheses tested are (I) different lineages within Woeseiales are associated with deep-sea or coastal environments, (II) they are a major component of the microbiome of deep-sea surface sediments, and (III) the genomic traits of the members of deep-sea lineage(s) indicate a chemoorganoheterotrophic lifestyle targeting complex detrital biomolecules

Methods

Results

Conclusion