Microbial consumption of zero-valence sulfur in marine benthic habitats

Summary Zero‐valence sulfur (S0) is a central intermediate in the marine sulfur cycle and forms conspicuous accumulations at sediment surfaces, hydrothermal vents and in oxygen minimum zones. Diverse microorganisms can utilize S0, but those consuming S0 in the environment are largely unknown. We ide...

Celý popis

Uložené v:

Podrobná bibliografia
Vydané v:	Environmental microbiology Ročník 16; číslo 11; s. 3416 - 3430
Hlavní autori:	Pjevac, Petra, Kamyshny Jr, Alexey, Dyksma, Stefan, Mußmann, Marc
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	England Blackwell Publishing Ltd 01.11.2014 Wiley Subscription Services, Inc
Predmet:	anaerobic conditions Anoxic conditions Biofilms Consumption Deep sea Deep water habitats Deltaproteobacteria - genetics Deltaproteobacteria - isolation & purification Deltaproteobacteria - metabolism Desulfobulbaceae Ecosystem Epsilonproteobacteria - genetics Epsilonproteobacteria - isolation & purification Epsilonproteobacteria - metabolism Geologic Sediments - chemistry habitats Hydrothermal Vents Marine microbial communities Microorganisms Ocean floor Oceans oxidants oxygen ribosomal RNA RNA, Ribosomal, 16S - genetics Seawater - microbiology sediments Sulfates - metabolism Sulfur Sulfur - analysis Sulfur - metabolism Sulfur cycle
ISSN:	1462-2912, 1462-2920, 1462-2920
On-line prístup:	Získať plný text
Tagy:	Pridať tag Žiadne tagy, Buďte prvý, kto otaguje tento záznam!

Popis
Shrnutí:	Summary Zero‐valence sulfur (S0) is a central intermediate in the marine sulfur cycle and forms conspicuous accumulations at sediment surfaces, hydrothermal vents and in oxygen minimum zones. Diverse microorganisms can utilize S0, but those consuming S0 in the environment are largely unknown. We identified possible key players in S0 turnover on native or introduced S0 in benthic coastal and deep‐sea habitats using the 16S ribosomal RNA approach, (in situ) growth experiments and activity measurements. In all habitats, the epsilonproteobacterial Sulfurimonas/Sulfurovum group accounted for a substantial fraction of the microbial community. Deltaproteobacterial Desulfobulbaceae and Desulfuromonadales were also frequently detected, indicating S0 disproportionation and S0 respiration under anoxic conditions. Sulfate production from S0 particles colonized in situ with Sulfurimonas/Sulfurovum suggested that this group oxidized S0. We also show that the type strain Sulfurimonas denitrificans is able to access cyclooctasulfur (S8), a metabolic feature not yet demonstrated for sulfur oxidizers. The ability to oxidize S0, in particular S8, likely facilitates niche partitioning among sulfur oxidizers in habitats with intense microbial sulfur cycling such as sulfidic sediment surfaces. Our results underscore the previously overlooked but central role of Sulfurimonas/Sulfurovum group for conversion of free S0 at the seafloor surface.
Bibliografia:	Cluster of Excellence MARUM ArticleID:EMI12410 istex:C3DA0F5F9F8C5D1DB0829171CF96AC8BF4F6639D ark:/67375/WNG-V4652JNM-B Max Planck Society Marie Curie Outgoing International Fellowship - No. POIF-GA-2008-219586 Fig. S1. (A) S0 precipitations in a sulfidic pool during low tide at the Janssand tidal flat (German Wadden Sea), (B) volcanogenic S0 boulder and (C) S0 outcrop at the North Su Volcano rising in the back-arc spreading centre Manus Basin (Bismarck Sea, Papua New Guinea), and (D) S0-precipitating microbial mat covering hydrothermal sediments in the Guaymas Basin (Gulf of California, Mexico).Fig. S2. Phylogenetic reconstruction of Epsilonproteobacteria-related 16S rRNA gene sequences using maximum likelihood (RAxML). Sequences were retrieved from particle-colonization experiments (Janssand 2010), from the S0-precipitating mat and from oxygen- and nitrate-respiring S0-enrichment cultures (Guaymas Basin). Representative OTUs (97% SI cut-off) were selected for presentation, n = number of sequences per OTU. Scale bar indicates 10% estimated sequence changes.Fig. S3. Phylogenetic reconstruction of Deltaproteobacteria-related 16S rRNA gene sequences using maximum likelihood (RAxML). Sequences were retrieved from particle-colonization experiments (Janssand 2010), from the S0-precipitating mat and from S0-respiring enrichment culture (Guaymas Basin). Sequences from S0-disproportionating cultures from Janssand tidal sediment and from Guaymas Basin sediments were provided by Kai Finster. Representative OTUs (97% SI cut-off) were selected for presentation, n = number of sequences per OTU. Scale bar indicates 10% estimated sequence changes.Fig. S4. (A) Epifluorescence images of DAPI-stained cells (in blue) in (a) S0-, (b) pyrite- and (c) glass-grown biofilms from the oxic sediment layer in Janssand tidal sediment (October 2010). Scale bar refers to 5 μm. (B) Epifluorescence images of (a) Epsilonproteobacteria (probe Epsy549) in a S0 biofilm from the oxic sediment layer, Janssand 2010, (b) Epsilonproteobacteria (Epsy914) accounting for up to 22% of DAPI in a S0-rich tidal pool (Janssand, May 2011), (c) Epsilonproteobacteria (probe mix Epsy549/Epsy914) in a volcanogenic S0 boulder (Manus Basin) and (d) Epsilonproteobacteria (probe mix Epsy549/Epsy914) and Arcobacter (inset, Arc94) in a S0-precipitating mat (Guaymas Basin). In green, CARD-FISH signal (Alexa 488); in blue, DAPI stain. Scale bar refers to 10 μm.Fig. S5. Epifluorescence images of Epsilonproteobacteria (probe Epsy549) in (A) oxygen- and (B) nitrate-respiring S0-enrichment cultures from the S0-precipitating microbial mat (Guaymas Basin). In green, CARD-FISH signal (Alexa 488); in blue, DAPI stain.Fig. S6. Sulfate production in (●) oxygen- and (◆) nitrate-respiring S0-enrichment cultures from the S0-precipitating microbial mat (Guaymas Basin).Fig. S7. Bathymetric map (Ocean Data View, ODV) of sampling locations in (A) tidal flats of the German Wadden Sea; (B) the Manus Basin back-arc spreading centre, Bismarck Sea, Papua New Guinea; (C) the Guaymas Basin, Gulf of California, Mexico. Map was constructed with help of Ocean Data View (Schlitzer, R., Ocean Data View, http://odv.awi.de, 2012.)Fig. S8. Detailed bathymetric map of the North Su sampling area (Manus Basin, Papua New Guinea). Volcanogenic S0 (yellow stars) and bottom water sample I (blue circle), active venting sites (gray circles). Scale bar indicates distance in meters. Figure adapted from Bach and colleagues (2011).Table S1. Semiquantitative relative abundance of Epsilonproteobacteria, Gammaproteobacteria and Deltaproteobacteria in biofilms grown on introduced S0, pyrite and glass particles in the Janssand tidal flat colonization experiment in October 2010, as determined by CARD-FISH. Legend: ++ abundant, + present, - absent. Table S2. Total cell counts (TCC, DAPI) and relative abundance (%) of selected populations determined by CARD-FISH in Janssand (JS, 2010; 2011) and Königshafen (KH, 2011) tidal sediments. Table S3. Sulfate (SO42-) production by S0-grown biofilms incubated in Königshafen tidal sediments (October 2011). Sulfate concentrations were calculated from IC measurements based on a Na2SO4 standard curve. Table S4. Details of sampling sites and dates, incubation periods and deposition/retrieval method. Table S5. Horseradish peroxidase-labelled oligonucleotide probes used for CARD-FISH. Table S6. Statistics of the 454-pyrotag data obtained from the NGS pipeline (SILVAngs) of the SILVA rRNA gene database project (Quast et al., 2013). Table S7. Sediment porosity, density and total extractable S0 (μmol g−1) used to calculate total S0 concentration in different sediment layers (Janssand, May 2011). Appendix S1. Supplementary methods. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23
ISSN:	1462-2912 1462-2920 1462-2920
DOI:	10.1111/1462-2920.12410