Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments

Abstract

Marine sediments are the largest carbon sink on earth. Nearly half of dark carbon fixation in the oceans occurs in coastal sediments, but the microorganisms responsible are largely unknown. By integrating the 16S rRNA approach, single-cell genomics, metagenomics and transcriptomics with 14 C-carbon assimilation experiments, we show that uncultured Gammaproteobacteria account for 70-86% of dark carbon fixation in coastal sediments. First, we surveyed the bacterial 16S rRNA gene diversity of 13 tidal and sublittoral sediments across Europe and Australia to identify ubiquitous core groups of Gammaproteobacteria mainly affiliating with sulfur-oxidizing bacteria. These also accounted for a substantial fraction of the microbial community in anoxic, 490-cm-deep subsurface sediments. We then quantified dark carbon fixation by scintillography of specific microbial populations extracted and flow-sorted from sediments that were short-term incubated with 14 Cbicarbonate. We identified three distinct gammaproteobacterial clades covering diversity ranges on family to order level (the Acidiferrobacter, JTB255 and SSr clades) that made up 450% of dark carbon fixation in a tidal sediment. Consistent with these activity measurements, environmental transcripts of sulfur oxidation and carbon fixation genes mainly affiliated with those of sulfur-oxidizing Gammaproteobacteria. The co-localization of key genes of sulfur and hydrogen oxidation pathways and their expression in genomes of uncultured Gammaproteobacteria illustrates an unknown metabolic plasticity for sulfur oxidizers in marine sediments. Given their global distribution and high abundance, we propose that a stable assemblage of metabolically flexible Gammaproteobacteria drives important parts of marine carbon and sulfur cycles.

Permeability shapes bacterial communities in sublittoral surface sediments

“…A). Members of this genus were highly abundant constituting up to 8% of total cells in tidal sediments in the North Sea (Lenk et al ., ) where they oxidize thiosulfate and sulfite, likely using oxygen as electron acceptor (Dyksma et al ., ). Woeseiaceae /JTB255 were present in all sublittoral North Sea sediments (1% to 6%) and comparably abundant as previously reported for European tidal sediments (3% to 6%).…”

Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment

“…2). In general, Lake Grevelingen surface sediments harbor a distinct microbial community comparable to other surface sediments, such as coastal marine (North Sea), estuarine, and Black Sea sediments (8,9,12), studied by 16S rRNA gene amplicon sequencing analysis.…”

“…Both chemolithoautotrophic sulfur-oxidizing Gammaproteobacteria and sulfur-disproportionating Deltaproteobacteria have been identified to play a major role in sulfur and carbon cycling in diverse intertidal sediments (10)(11)(12). Hence, chemolithoautotrophic sulfur-oxidizing communities vary between sediment environments, but it is presently not clear as to which environmental factors are actually determining the chemolithoautotrophic community composition at a given site.…”

Microbial community assembly in marine sediments

“…While universally prevalent, many of these taxa appear to predominate at different depths within the sediment column. Analyses of surface sediment are marked by a higher percentage of proteobacterial classes (Gamma-, Delta-, and Alphaproteobacteria) (Li et al 2009, Quaiser et al 2011, Zinger et al 2011, Hamdan et al 2013, Dyksma et al 2016, while the subsurface is often dominated by sequences clustering within the Atribacteria and the 3 archaeal phyla mentioned in the previous paragraph (Teske 2006, Orcutt et al 2011, Parkes et al 2014. Analyses of the factors underlying these distribution patterns have proposed varying theories.…”