Biodegradation of low-molecular-weight alkanes under mesophilic, sulfate-reducing conditions: metabolic intermediates and community patterns

Abstract

We evaluated the ability of the native microbiota in a low-temperature, sulfidic natural hydrocarbon seep (Zodletone) to metabolize short-chain hydrocarbons. n-Propane and n-pentane were metabolized under sulfate-reducing conditions in initial enrichments and in sediment-free subcultures. Carbon isotope analysis of residual propane in active enrichments showed that propane became enriched in (13)C by 6.7 (+/-2.0) per thousand, indicating a biological mechanism for propane loss. The detection of n-propylsuccinic and isopropylsuccinic acids in active propane-degrading enrichments provided evidence for anaerobic biodegradation via a fumarate addition pathway. A eubacterial 16S rRNA gene survey of sediment-free enrichments showed that the majority of the sequenced clones were phylogenetically affiliated within the Deltaproteobacteria. Such sequences were most closely affiliated with clones retrieved from hydrocarbon-impacted marine ecosystems, volatile fatty acid metabolizers, hydrogen users, and with a novel Deltaproteobacterial lineage. Other cloned sequences were affiliated with the Firmicutes and Chloroflexi phyla. The sequenced clones were only distantly (<95%) related to other reported low-molecular-weight alkane-degrading sulfate-reducing populations. This work documents the potential for anaerobic short-chain n-alkane metabolism for the first time in a terrestrial environment, provides evidence for a fumarate addition mechanism for n-propane activation under these conditions, and reveals microbial community members present in such enrichments.

Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps

“…The oxidation of non-methane alkanes with sulfate has recently been reported to occur across a range of temperatures in diverse marine and terrestrial seeps or vents (e.g. Joye et al, 2004;Kniemeyer et al, 2007;Orcutt et al, 2010;Savage et al, 2010;Quistad and Valentine, 2011;Jaekel et al, 2012;Adams et al, 2013;Bose et al, 2013). Measured rates of alkane degradation and SR closely followed stoichiometric predictions that assume complete oxidation of alkanes to CO 2 (e.g.…”

Anaerobic degradation of propane and butane by sulfate-reducing bacteria enriched from marine hydrocarbon cold seeps

“…Quantitative growth experiments showed that the enrichment cultures degraded propane or butane completely to CO 2 , with stoichiometric reduction of sulfate to sulfide, as described before (Kniemeyer et al, 2007;Savage et al, 2010). The enrichment cultures were tested for their ability to degrade methane, the dominant hydrocarbon at gas seeps and other alkanes found in relatively high concentrations in such environments, for example, ethane, isobutane and pentane.…”

“…In addition, oxidation of propane under anoxic conditions has been determined in sediments collected from marine gas seeps (Quistad and Valentine, 2011). Anaerobic degradation of shortchain alkanes was demonstrated recently with a pure culture of a marine sulfate-reducing bacterium strain BuS5, isolated from Guaymas Basin hydrothermal vent sediments (Kniemeyer et al, 2007), and with several enrichment cultures obtained from sediments around marine and terrestrial hydrocarbon seeps (Kniemeyer et al, 2007;Savage et al, 2010). Strain BuS5 can degrade both propane and butane and is phylogenetically affiliated with the Desulfosarcina-Desulfococcus cluster of the Deltaproteobacteria.…”

“…Strain BuS5 can degrade both propane and butane and is phylogenetically affiliated with the Desulfosarcina-Desulfococcus cluster of the Deltaproteobacteria. Analysis of metabolites showed that propane and butane are activated similar to higher alkanes by addition to fumarate (Kropp et al, 2000;Rabus et al, 2001) primarily at the secondary carbon atom yielding iso-propyl-and (1-methylpropyl)-succinate, respectively (Kniemeyer et al, 2007;Savage et al, 2010).…”

Dechlorination of p,p′-DDTs coupled with sulfate reduction by novel sulfate-reducing bacterium Clostridium sp. BXM

“…During this reductive dechlorination process, RSCs served as nucleophilic reductants and/ or electron donor, and ultimately transformed into oxidized sulfur compounds (OSCs) (Zheng et al, 2006). Besides the level of sulfate, the amended organic material which serves as both electron donor and carbon source (Savage et al, 2010) was another limiting factor for the generation of RSCs. SRB can utilize an impressive array of organic matter to support their metabolic activity (Zhang and Young, 1997;Aeckersberg et al,1998).…”