Abstract
Sulfate-reducing microorganisms (SRMs) often compete with methanogens for common substrates. Due to thermodynamic reasons, SRMs should outcompete methanogens in the presence of sulfate. However, many studies have documented coexistence of these microbial groups in natural environments, suggesting that thermodynamics alone cannot explain the interactions among them. In this study, we investigated how SRMs compete with the established methanogenic communities in sediment from a long-term, electron acceptor-depleted, asphalt-exposed ecosystem and how they affect the composition of the organic material. We hypothesized that, upon addition of sulfate, SRMs (i) outcompete the methanogenic communities and (ii) markedly contribute to transformations of the organic material. We sampled sediments from the test and proximate control sites under anoxic conditions and incubated them in seawater medium with or without sulfate. Abundance and activity pattern of SRMs and methanogens, as well as the total prokaryotic community, were followed for 6 weeks by using qPCR targeting selected marker genes. Some of these genes were also subjected to amplicon sequencing to assess potential shifts in diversity patterns. Alterations of the organic material in the microcosms were determined by mass spectrometry. Our results indicate that the competition of SRMs with methanogens upon sulfate addition strongly depends on the environment studied and the starting microbiome composition. In the asphalt-free sediments (control), the availability of easily degradable organic material (mainly plant-derived) allows SRMs to use a larger variety of substrates, reducing interspecies competition with methanogens. In contrast, the abundant presence of recalcitrant compounds in the asphalt-exposed sediment was associated with a strong competition between SRMs and methanogens, ultimately detrimental for the latter. Our data underpin the importance of the quality of bioavailable organic materials in anoxic environments as a driver for microbial community structure and function.
Highlights
Sulfate-reducing microorganisms are anaerobic prokaryotes that use dissimilatory sulfate reduction to conserve energy and sustain their growth
The abundance of sulfate-reducing microorganisms (SRMs) and methanogens was comparable on day 0 in the N microcosms, while in the H microcosms methanogens were higher in abundance compared to SRMs at the same time point
All detected genes gradually increased in abundance and peaked on day 16 in the N microcosms, with a higher increase of bacterial 16S rRNA, dsrB and bamA genes observed in the non-exposed sediment with sulfate (NS), compared to non-exposed sediment without sulfate (NC)
Summary
Sulfate-reducing microorganisms are anaerobic prokaryotes that use dissimilatory sulfate reduction to conserve energy and sustain their growth. The transfer of electrons to sulfate (SO42−) leads to sulfide (S2−) formation and yields considerably less energy compared to other energy-conserving pathways (Thauer et al, 1977) Despite their energetic disadvantage and accompanying low growth rates, SRMs have been detected in various environments and have a significant impact on the sulfur and carbon cycles (Rabus et al, 2015). In the presence of sulfate, SRMs are expected to outcompete methanogens in anoxic environments They have a higher affinity for H2 and acetate (Oude Elferink et al, 1994; Omil et al, 1998), the main substrates for hydrogenotrophic and acetogenic methanogens, respectively, and a higher energy yield compared to methanogenesis (McInerney et al, 2009; Bethke et al, 2011).
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