Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria

Abstract

The short-chain hydrocarbons ethane, propane and butane are constituents of natural gas. They are usually assumed to be of thermochemical origin, but biological formation of ethane and propane has been also observed. Microbial utilization of short-chain hydrocarbons has been shown in some aerobic species but not in anaerobic species of bacteria. On the other hand, anaerobic utilization of short-chain hydrocarbons would in principle be expected because various anaerobic bacteria grow with higher homologues (> or =C(6)). Indeed, chemical analyses of hydrocarbon-rich habitats with limited or no access of oxygen indicated in situ biodegradation of short-chain hydrocarbons. Here we report the enrichment of sulphate-reducing bacteria (SRB) with such capacity from marine hydrocarbon seep areas. Propane or n-butane as the sole growth substrate led to sediment-free sulphate-reducing enrichment cultures growing at 12, 28 or 60 degrees C. With ethane, a slower enrichment with residual sediment was obtained at 12 degrees C. Isolation experiments resulted in a mesophilic pure culture (strain BuS5) that used only propane and n-butane (methane, isobutane, alcohols or carboxylic acids did not support growth). Complete hydrocarbon oxidation to CO2 and the preferential oxidation of 12C-enriched alkanes were observed with strain BuS5 and other cultures. Metabolites of propane included iso- and n-propylsuccinate, indicating a subterminal as well as an unprecedented terminal alkane activation with involvement of fumarate. According to 16S ribosomal RNA analyses, strain BuS5 affiliates with Desulfosarcina/Desulfococcus, a cluster of widespread marine SRB. An enrichment culture with propane growing at 60 degrees C was dominated by Desulfotomaculum-like SRB. Our results suggest that diverse SRB are able to thrive in seep areas and gas reservoirs on propane and butane, thus altering the gas composition and contributing to sulphide production.

Molecular and isotopic partitioning of low-molecular-weight hydrocarbons during migration and gas hydrate precipitation in deposits of a high-flux seepage site

“…Indications for microbial consumption of propane, i.e., considerable removal accompanied by slight 13 C-enrichments of the residual propane in type I ss and type IIa gas compared to vent gas (type IIb vg ) were found as well. C 2 /C 3 ratios higher in type I ss compared to type IIa gas (Table 2) indicate additional propane depletion in shallow sediments, as previously reported for shallow deposits of mud volcanoes in the Sorokin Trough (Stadnitskaia et al, 2008), possibly owing to its concurrent microbial consumption (Kniemeyer et al, 2007). However, as propane depletions due to size exclusion during hydrate precipitations are also known , the specific effects of the aforementioned abiotic and biotic processes leading to propane removal are uncertain.…”

“…This process is considered to preferentially attack LMWHC with secondary carbon atoms in sub-terminal positions relative to those with tertiary or quaternary sub-terminal carbons (Boreham et al, 2008). Hence, C 3 , and linear C 4 and C 5 -alkanes are typically transformed by hydrocarbon degraders, whereas C 2 and iso-C 4 appear to be less affected or even remain unaltered (Head et al, 2003;Horstad and Larter, 1997;James and Burns, 1984;Kniemeyer et al, 2007;Larter and di Primio, 2005;Stadnitskaia et al, 2006). Typically, anaerobic microbial degradation of wet gas LMWHC (C 2+ ) by electron acceptors other than sulfate (Widdel and Rabus, 2001;Zengler et al, 1999) leads to addition of 13 C-enriched, secondary methane (Milkov and Dzou, 2007).…”

“…These include i) biological degradation of individual compounds (James and Burns, 1984;Kniemeyer et al, 2007;Larter and di Primio, 2005;Pallasser, 2000), ii) preferential incorporation into hydrate cages (Sloan and Koh, 2007), iii) admixture of secondary volatiles derived from degradation of oil (Milkov and Dzou, 2007;Prinzhofer and Pernaton, 1997;Seewald, 2003), and iv) preferential methane consumption mediated by the anaerobic oxidation of methane (AOM) in top sediments (Barnes and Goldberg, 1976;Hinrichs and Boetius, 2002;Hoehler et al, 1994;Reeburgh, 1976). Considering the different alteration effects associated with upward migration and partitioning, the molecular and isotopic composition of LMWHC in shallow sedimentary pools or in vent gas can deviate from the source gas of the reservoir.…”

Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples

“…Indeed, all of the known strictly anaerobic (for example, sulfate-reducing/syntrophic) alkane degraders are Deltaproteobacteria (Mbadinga et al, 2011;Agrawal and Gieg, 2013;Callaghan, 2013). However, the implication of a Peptococcaceae in degradation of low molecular weight n-alkanes (for example, propane) under sulfate-reducing conditions (Kniemeyer et al, 2007) and iso-alkanes under methanogenic conditions (Abu Laban et al, in press; Tan et al, 2014B) supports a role for Firmicutes in anaerobic alkane degradation. Based on the dominant OTUs in these cultures and the phylogenetic distribution of genes involved in fumarate addition, the primary hydrocarbon degraders in NAPDC, SCADC and TOLDC appeared to consist of different species from a few bacterial taxa (Table 3; Supplementary Figure S3).…”

Identification of chlorinated solvents degradation zones in clay till by high resolution chemical, microbial and compound specific isotope analysis

“…Potentially, ethene could be produced in the entire sub-section above 6.22 m b.s. However, microbial oxidation during sulfate or iron reduction (Kniemeyer et al, 2007) or diffusive loss to fractures may have resulted in ethene depletion. Degradation of TCE and cis-DCE in the sub-section is documented by the enriched δ 13 C values for TCE and cis-DCE (Fig.…”