Anaerobic oxidation of short-chain alkanes in hydrothermal sediments: potential influences on sulfur cycling and microbial diversity

Abstract

Short-chain alkanes play a substantial role in carbon and sulfur cycling at hydrocarbon-rich environments globally, yet few studies have examined the metabolism of ethane (C2), propane (C3), and butane (C4) in anoxic sediments in contrast to methane (C1). In hydrothermal vent systems, short-chain alkanes are formed over relatively short geological time scales via thermogenic processes and often exist at high concentrations. The sediment-covered hydrothermal vent systems at Middle Valley (MV, Juan de Fuca Ridge) are an ideal site for investigating the anaerobic oxidation of C1–C4 alkanes, given the elevated temperatures and dissolved hydrocarbon species characteristic of these metalliferous sediments. We examined whether MV microbial communities oxidized C1–C4 alkanes under mesophilic to thermophilic sulfate-reducing conditions. Here we present data from discrete temperature (25, 55, and 75°C) anaerobic batch reactor incubations of MV sediments supplemented with individual alkanes. Co-registered alkane consumption and sulfate reduction (SR) measurements provide clear evidence for C1–C4 alkane oxidation linked to SR over time and across temperatures. In these anaerobic batch reactor sediments, 16S ribosomal RNA pyrosequencing revealed that Deltaproteobacteria, particularly a novel sulfate-reducing lineage, were the likely phylotypes mediating the oxidation of C2–C4 alkanes. Maximum C1–C4 alkane oxidation rates occurred at 55°C, which reflects the mid-core sediment temperature profile and corroborates previous studies of rate maxima for the anaerobic oxidation of methane (AOM). Of the alkanes investigated, C3 was oxidized at the highest rate over time, then C4, C2, and C1, respectively. The implications of these results are discussed with respect to the potential competition between the anaerobic oxidation of C2–C4alkanes with AOM for available oxidants and the influence on the fate of C1 derived from these hydrothermal systems.

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.…”

“…Joye et al, 2004;Kniemeyer et al, 2007;Orcutt et al, 2010;Bowles et al, 2011;Quistad and Valentine, 2011;Bose et al, 2013) and isolates or enrichment cultures of hydrocarbon-degrading SRB (e.g. Kniemeyer et al, 2007;Jaekel et al, 2012;Adams et al, 2013;Bose et al, 2013). Here, we provide the direct link between biogeochemical patterns and apparently specialized DSS subclades of key alkane degraders in marine sediments.…”

“…see Quistad and Valentine, 2011;Bose et al, 2013). Reported rates for anaerobic short-chain alkane (SCA) oxidation were high in alkane-amended slurries of Gulf of Mexico or Middle Valley sediments (34-354 nmol C 2 -C 4 ml À 1 per day; Adams et al, 2013;Bose et al, 2013). In situ anaerobic propane oxidation rates in fresh sediments from a gas seep located in the Santa Barbara Channel even exceeded rates from the batch cultures with up to 2100 nmol propane cm À 3 per day (Quistad and Valentine, 2011).…”

Volatile organic compounds (VOCs) in soil gases from Solfatara crater (Campi Flegrei, southern Italy): Geogenic source(s) vs. biogeochemical processes

“…Soils may also represent an important source for various VOCs, including alkanes (Mackie and Wheatley, 1999;Asensio et al, 2007;Bunge et al, 2008;Leff and Fierer, 2008). In hydrothermal environments, alkane degradation to CO 2 was found to proceed through thermal alteration of organic matter buried in sediments interacting with hydrothermal fluids Seewald, 2006, 2010), a process that may be dependent on sulfate reduction (Kniemeyer et al, 2007;Adams et al, 2013;Jaekel et al, 2013). In these natural systems, abiotic synthesis through Fischer-Tropsch reactions may produce significant amounts of alkanes (Sherwood Lollar et al, 2002;Proskurowski et al, 2008), although these compounds are considered mostly biogenic (McCollom, 2013).…”

Abyssivirga alkaniphila gen. nov., sp. nov., an alkane-degrading, anaerobic bacterium from a deep-sea hydrothermal vent system, and emended descriptions of Natranaerovirga pectinivora and Natranaerovirga hydrolytica

“…High concentrations of ammonium and methane in the end-member fluids indicate that the system is sediment influenced. The sediment influence makes formation of higher hydrocarbons plausible in the LCVF, as in the Guaymas Basin (Bazylinski et al, 1989) and the Middle Valley vent fields at the Juan de Fuca Ridge (Adams et al, 2013). Measurements of complex hydrocarbons have not been performed in hydrothermal fluids from the LCVF.…”