Cable bacteria promote DNRA through iron sulfide dissolution

Kessler, Adam J.; Wawryk, Michaela; Marzocchi, Ugo; Roberts, Keryn L.; Wong, Wei Wen; Risgaard-Petersen, Nils; Meysman, Filip J. R.; Glud, Ronnie N.; Cook, Perran

doi:10.1002/lno.11110

Cited by 44 publications

(27 citation statements)

References 60 publications

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“…Similar partitioning of the two dissimilative NO 3 − -reducing processes, with a relatively large contribution of DNRA has been observed in a wide range of environments, particularly in reduced sediments with high organic matter content and comparatively low nitrate levels (Burgin and Hamilton, 2007;Dong et al, 2011). The contribution of DNRA to total NO 3 − reduction can be particularly important in both estuarine sediments (∼5-91%; An and Gardner, 2002;Megonigal et al, 2004;Gardner et al, 2006;Burgin and Hamilton, 2007;Dong et al, 2009;Giblin et al, 2013;Roberts et al, 2014;Plummer et al, 2015;Kessler et al, 2019) and freshwater lake sediments (∼3-50%; Nizzoli et al, 2010;Wenk et al, 2014;Robertson and Thamdrup, 2017). Yet, the natural variability in these studied environments is quite high.…”

Section: Discussion Denitrification Versus Dnra In Lake Lugano Sedimentssupporting

confidence: 52%

Controls of H2S, Fe2 +, and Mn2 + on Microbial NO3–-Reducing Processes in Sediments of an Eutrophic Lake

et al. 2020

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Understanding the biogeochemical controls on the partitioning between nitrogen (N) removal through denitrification and anaerobic ammonium oxidation (anammox), and N recycling via dissimilatory nitrate (NO 3 −) reduction to ammonium (DNRA) is crucial for constraining lacustrine N budgets. Besides organic carbon, inorganic compounds may serve as electron donors for NO 3 − reduction, yet the significance of lithotrophic NO 3 − reduction in the environment is still poorly understood. Conducting incubation experiments with additions of 15 N-labeled compounds and reduced inorganic substrates (H 2 S, Fe 2+ , Mn 2+), we assessed the role of alternative electron donors in regulating the partitioning between the different NO 3 −-reducing processes in ferruginous surface sediments of Lake Lugano, Switzerland. In sediment slurry incubations without added inorganic substrates, denitrification and DNRA were the dominant NO 3 −-reducing pathways, with DNRA contributing between 31 and 46% to the total NO 3 − reduction. The contribution of anammox was less than 1%. Denitrification rates were stimulated by low to moderate additions of ferrous iron (Fe 2+ ≤ 258 µM) but almost completely suppressed at higher levels (≥1300 µM). Conversely, DNRA was stimulated only at higher Fe 2+ concentrations. Dissolved sulfide (H 2 S, i.e., sum of H 2 S, HS − and S 2−) concentrations up to ∼80 µM, strongly stimulated denitrification, but did not affect DNRA significantly. At higher H 2 S levels (≥125 µM), both processes were inhibited. We were unable to find clear evidence for Mn 2+-supported lithotrophic NO 3 − reduction. However, at high concentrations (∼500 µM), Mn 2+ additions inhibited NO 3 − reduction, while it did not affect the balance between the two NO 3 − reduction pathways. Our results provide experimental evidence for chemolithotrophic denitrification or DNRA with Fe 2+ and H 2 S in the Lake Lugano sediments, and demonstrate that all tested potential electron donors, despite the beneficial effect at low concentrations of some of them, can inhibit NO 3 − reduction at high concentration levels. Our findings thus imply that the concentration of inorganic electron donors in lake sediments can act as an important regulator of both benthic denitrification and DNRA rates, and suggest that they can exert an important control on the relative partitioning between microbial N removal and N retention in lakes.

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Section: Discussion Denitrification Versus Dnra In Lake Lugano Sedimentssupporting

confidence: 52%

Controls of H2S, Fe2 +, and Mn2 + on Microbial NO3–-Reducing Processes in Sediments of an Eutrophic Lake

et al. 2020

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“…Desulfobulbaceae include organisms known as cable bacteria that are capable of sulphur oxidation with either oxygen (Nielsen et al, 2010;Pfeffer et al, 2012) or nitrate (Marzocchi et al, 2014;Kessler et al, 2018Kessler et al, , 2019 as electron acceptors. In addition to their role as sulphide oxidizers, a recent study showed cable bacteria enhanced the relative importance of DNRA by increasing Fe 2+ availability (via decreasing the pH which allowed FeS dissolution) that promoted other microbes in the community to conduct Fe-dependent DNRA (Kessler et al, 2019). However, in our experiment, only one Desulfobulbaceae ASV, that had no assigned Genus using the Silva database, closely matched a cable bacteria genus (Candidate genus Electrothrix (Trojan et al, 2016)] [>95% identity, NCBI's nucleotide collection database (Agarwala et al, 2018)].…”

Section: Evidence Of Sulphide Oxidation Under High P Sulphidementioning

confidence: 99%

Sulphide addition favours respiratory ammonification (DNRA) over complete denitrification and alters the active microbial community in salt marsh sediments

Murphy

Bulseco

Ackerman

et al. 2020

Environmental Microbiology

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The balance between nitrate respiration pathways, denitrification and dissimilatory nitrate (NO 3 − ) reduction to ammonium (DNRA), determines whether bioavailable nitrogen is removed as N 2 gas or recycled as ammonium. Saltwater intrusion and organic matter enrichment may increase sulphate reduction leading to sulphide accumulation. We investigated the effects of sulphide on the partitioning of NO 3 − between complete denitrification and DNRA and the microbial communities in salt marsh sediments. Complete denitrification significantly decreased with increasing sulphide, resulting in an increase in the contribution of DNRA to NO 3 − respiration. Alternative fates of NO 3 − became increasingly important at higher sulphide treatments, which could include N 2 O production and/or transport into intracellular vacuoles. Higher 16S transcript diversity was observed in the high sulphide treatment, with clear shifts in composition. Generally, low and no sulphide, coupled with high NO 3 − , favoured the activity of Campylobacterales, Oceanospirillales and Altermonadales, all of which include opportunistic denitrifiers. High P sulphide conditions promoted the activity of potential sulphide oxidizing nitrate reducers (Desulfobulbaceae, Acidiferrobacteraceae and Xanthomonadales) and sulphate reducers (Desulfomonadaceae, Desulfobacteraceae). Our study highlights the tight coupling between N and S cycling, and the implications of these dynamics on the fate of bioavailable N in coastal environments susceptible to intermittent saltwater inundation and organic matter enrichment.Received

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“…It has been suggested that when long filaments form, a chain of cells at the sulfidic terminal catalyzes anodic half reactions (e.g., 0.5 H 2 S + 2H 2 O → 0.5 SO 2− 4 + 4e − + 5H + ), while a cathodic half reaction (O 2 + 4e − + 4H + → 2H 2 O) is completed by cells at the oxic terminal. Electron transfer then occurs along the lon-gitudinal ridges of CB filaments via electron hopping promoted by extracellular cytochromes positioned within a redox gradient or via conductive electronic structures such as pili (Bjerg et al, 2018;Cornelissen et al, 2018;Kjeldsen et al, 2019;Meysman et al, 2019;Pfeffer et al, 2012). These hypotheses await further verification, and CB remain uncultured and difficult to grow outside of sediment.…”

Section: Introductionmentioning

confidence: 99%

Inducing the attachment of cable bacteria on oxidizing electrodes

Reimers

Alleau

2020

Biogeosciences

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Abstract. Cable bacteria (CB) are multicellular, filamentous bacteria within the family of Desulfobulbaceae that transfer electrons longitudinally from cell to cell to couple sulfide oxidation and oxygen reduction in surficial aquatic sediments. In the present study, electrochemical reactors that contain natural sediments are introduced as a tool for investigating the growth of CB on electrodes poised at an oxidizing potential. Our experiments utilized sediments from Yaquina Bay, Oregon, USA, and we include new phylogenetic analyses of separated filaments to confirm that CB from this marine location cluster with the genus “Candidatus Electrothrix”. These CB may belong to a distinctive lineage, however, because their filaments contain smaller cells and a lower number of longitudinal ridges compared to cables described from other locales. The results of a 135 d bioelectrochemical reactor experiment confirmed that these CB can migrate out of reducing sediments and grow on oxidatively poised electrodes suspended in anaerobic seawater. CB filaments and several other morphologies of Desulfobulbaceae cells were observed by scanning electron microscopy and fluorescence in situ hybridization on electrode surfaces, albeit in low densities and often obscured by mineral precipitation. These findings provide new information to suggest what kinds of conditions will induce CB to perform electron donation to an electrode surface, further informing future experiments to culture CB outside of a sediment matrix.

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Cable bacteria promote DNRA through iron sulfide dissolution

Cited by 44 publications

References 60 publications

Controls of H2S, Fe2 +, and Mn2 + on Microbial NO3–-Reducing Processes in Sediments of an Eutrophic Lake

Controls of H2S, Fe2 +, and Mn2 + on Microbial NO3–-Reducing Processes in Sediments of an Eutrophic Lake

Sulphide addition favours respiratory ammonification (DNRA) over complete denitrification and alters the active microbial community in salt marsh sediments

Inducing the attachment of cable bacteria on oxidizing electrodes

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