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Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community.

ABSTRACT: Stimulation of subsurface microorganisms to induce reductive immobilization of metals is a promising approach for bioremediation, yet the overall microbial community response is typically poorly understood. Here we used proteogenomics to test the hypothesis that excess input of acetate activates complex community functioning and syntrophic interactions among autotrophs and heterotrophs. A flow-through sediment column was incubated in a groundwater well of an acetate-amended aquifer and recovered during microbial sulfate reduction. De novo reconstruction of community sequences yielded near-complete genomes of Desulfobacter (Deltaproteobacteria), Sulfurovum- and Sulfurimonas-like Epsilonproteobacteria and Bacteroidetes. Partial genomes were obtained for Clostridiales (Firmicutes) and Desulfuromonadales-like Deltaproteobacteria. The majority of proteins identified by mass spectrometry corresponded to Desulfobacter-like species, and demonstrate the role of this organism in sulfate reduction (Dsr and APS), nitrogen fixation and acetate oxidation to CO2 during amendment. Results indicate less abundant Desulfuromonadales, and possibly Bacteroidetes, also actively contributed to CO2 production via the tricarboxylic acid (TCA) cycle. Proteomic data indicate that sulfide was partially re-oxidized by Epsilonproteobacteria through nitrate-dependent sulfide oxidation (using Nap, Nir, Nos, SQR and Sox), with CO2 fixed using the reverse TCA cycle. We infer that high acetate concentrations, aimed at stimulating anaerobic heterotrophy, led to the co-enrichment of, and carbon fixation in Epsilonproteobacteria. Results give an insight into ecosystem behavior following addition of simple organic carbon to the subsurface, and demonstrate a range of biological processes and community interactions were stimulated.

SUBMITTER: Handley KM

PROVIDER: S-EPMC3603403 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community.

Handley Kim M KM VerBerkmoes Nathan C NC Steefel Carl I CI Williams Kenneth H KH Sharon Itai I Miller Christopher S CS Frischkorn Kyle R KR Chourey Karuna K Thomas Brian C BC Shah Manesh B MB Long Philip E PE Hettich Robert L RL Banfield Jillian F JF

The ISME journal 20121129 4

Stimulation of subsurface microorganisms to induce reductive immobilization of metals is a promising approach for bioremediation, yet the overall microbial community response is typically poorly understood. Here we used proteogenomics to test the hypothesis that excess input of acetate activates complex community functioning and syntrophic interactions among autotrophs and heterotrophs. A flow-through sediment column was incubated in a groundwater well of an acetate-amended aquifer and recovered ...[more]

PMID: 23190730

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Project description:Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.

Project description:Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) is a high explosive released to the environment as a result of weapons manufacturing and testing worldwide. At Los Alamos National Laboratory, the Technical Area (TA) 16 260 Outfall discharged high-explosives-bearing water from a high-explosives-machining facility to Cañon de Valle during 1951 through 1996. These discharges served as a primary source of high-explosives and inorganic-element contamination in the area. Data indicate that springs, surface water, alluvial groundwater, and perched-intermediate groundwater contain explosive compounds, including RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine); HMX (octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine); and TNT (2,4,6-trinitrotoluene). RDX has been detected in the regional aquifer in several wells, and a corrective measures evaluation is planned to identify remedial alternatives to protect the regional aquifer. Perched-intermediate groundwater at Technical Area 16 is present at depths from 650 ft to 1200 ft bgs. In this study, we examined the microbial diversity in a monitoring well completed in perched-intermediate groundwater contaminated by RDX, and examined the response of the microbial population to biostimulation under varying geochemical conditions. Results show that the groundwater microbiome was dominated by Actinobacteria and Proteobacteria. A total of 1,605 operational taxonomic units (OTUs) in 96 bacterial genera were identified. Rhodococcus was the most abundant genus (30.6%) and a total of 46 OTUs were annotated as Rhodococcus. One OTU comprising 25.2% of total sequences was closely related to a RDX -degrading strain R. erythropolis HS4. A less abundant OTU from the Pseudomonas family closely related to RDX-degrading strain P. putida II-B was also present. Biostimulation significantly enriched Proteobacteria but decreased/eliminated the population of Actinobacteria. Consistent with RDX degradation, the OTU closely related to the RDX-degrading P. putida strain II-B was specifically enriched in the RDX-degrading samples. Analysis of the accumulation of RDX-degradation products reveals that during active RDX degradation, there is a transient increase in the concentration of the degradation products MNX, DNX, TNX, and NDAB. The accumulation of these degradation products suggests that RDX is degraded via sequential reduction of the nitro functional groups followed by abiotic ring-cleavage. The results suggest that strict anaerobic conditions are needed to stimulate RDX degradation under the TA-16 site-specific conditions.

Dataset Information

Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community.

Publications

Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community.

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