Microbial Communities in Methane- and Short Chain Alkane-Rich Hydrothermal Sediments of Guaymas Basin

Abstract

The hydrothermal sediments of Guaymas Basin, an active spreading center in the Gulf of California (Mexico), are rich in porewater methane, short-chain alkanes, sulfate and sulfide, and provide a model system to explore habitat preferences of microorganisms, including sulfate-dependent, methane- and short chain alkane-oxidizing microbial communities. In this study, hot sediments (above 60°C) covered with sulfur-oxidizing microbial mats surrounding a hydrothermal mound (termed “Mat Mound”) were characterized by porewater geochemistry of methane, C2–C6 short-chain alkanes, sulfate, sulfide, sulfate reduction rate measurements, in situ temperature gradients, bacterial and archaeal 16S rRNA gene clone libraries and V6 tag pyrosequencing. The most abundantly detected groups in the Mat mound sediments include anaerobic methane-oxidizing archaea of the ANME-1 lineage and its sister clade ANME-1Guaymas, the uncultured bacterial groups SEEP-SRB2 within the Deltaproteobacteria and the separately branching HotSeep-1 Group; these uncultured bacteria are candidates for sulfate-reducing alkane oxidation and for sulfate-reducing syntrophy with ANME archaea. The archaeal dataset indicates distinct habitat preferences for ANME-1, ANME-1-Guaymas, and ANME-2 archaea in Guaymas Basin hydrothermal sediments. The bacterial groups SEEP-SRB2 and HotSeep-1 co-occur with ANME-1 and ANME-1Guaymas in hydrothermally active sediments underneath microbial mats in Guaymas Basin. We propose the working hypothesis that this mixed bacterial and archaeal community catalyzes the oxidation of both methane and short-chain alkanes, and constitutes a microbial community signature that is characteristic for hydrothermal and/or cold seep sediments containing both substrates.

Defining boundaries for the distribution of microbial communities beneath the sediment-buried, hydrothermally active seafloor

“…In this study, all of the pore-water geochemical analyses, metabolic activity measurements and cellular and molecular microbial community analyses indicated the occurrence of functionally active microbial communities dominated by AOM populations in the relatively shallow subseafloor habitats down to 15.8 mbsf in Hole C0014G. Several studies have examined the abundance, phylogenetic diversity and function of AOM populations associated with seafloor hydrothermal activity in the Guaymas Basin and Yonaguni Knoll IV fields (Teske et al, 2002;Nunoura et al, 2010;Yanagawa et al, 2013a;Dowell et al, 2016). Because these investigations have focused on the shallow sediments just beneath the seafloor, where the diffusive mixing of hydrothermal fluids and seawater likely characterizes the geochemical environments, there remains a lack of knowledge on the subseafloor AOM communities associated with hydrogeologically controlled advection and the partitioning and mixing processes of hydrothermal fluids and infiltrated seawater near deep-sea vents.…”

“…(Supplementary Data S1). The HotSeep-1 group was previously detected in hydrothermal sediments in the Guaymas Basin (Teske et al, 2002;Kniemeyer et al, 2007;Dowell et al, 2016) and in an enrichment culture of anaerobic methane oxidizers Figure 3 16S rRNA gene phylotype compositions in the sediments from Site C0014, displayed (a) with respect to sediment depth using a universal primer set (Uni530F-907R) and (b) as pie diagrams at specific depths using an archaea-specific primer set (Arc530F-Arc958R). Archaeal 16S rRNA gene amplicons were obtained from three samples, which were not amplified with Uni530F-907R (shown as 'ND' in the black column).…”

“…Several studies have further addressed the potential microbial habitats beneath the seafloor hydrothermal vents, the so-called 'sub-vent biosphere', and have indicated the possible occurrence of functionally active and metabolically diverse (hyper-)thermophilic microbial communities associated with shallow subseafloor hydrothermal fluids and mineral deposits (Deming and Baross, 1993;Delaney et al, 1998;Summit and Baross, 1998;Huber et al, 2002Huber et al, , 2003. The compositions and functions of the sub-vent microbial communities have been inferred from culture-dependent and culture-independent analyses of microbial communities in (i) in situ growth chambers placed in hydrothermal fluid flows (Karl et al, 1988;Reysenbach et al, 2000;Corre et al, 2001;Takai et al, 2004), (ii) crustal fluids collected directly from the shallow subseafloor environments (~10 m below the seafloor [mbsf]) via seafloor drilling or probe insertion (Cowen et al, 2003;Higashi et al, 2004;Huber et al, 2006;Kato et al, 2009;Orcutt et al, 2011), (iii) hydrothermal sediments (Teske et al, 2002;Dhillon et al, 2005;Nunoura et al, 2010;Teske et al, 2014;Dowell et al, 2016;Teske et al, 2016) and (iv) chimney structures of active hydrothermal vents (Takai et al, 2001;Schrenk et al, 2003;Nakagawa et al, 2005). These studies found that mesophilic, thermophilic and hyperthermophilic members of Epsilonproteobacteria, Gammaproteobacteria, Aquificales, Thermococcales and Methanococales were the potentially predominant microbial components in the sub-vent biosphere.…”

Hydrothermal activity lowers trophic diversity in Antarctic sedimented hydrothermal vents

“…This creates opportunities for non-specialist, soft-sediment fauna to 38 colonise areas of chemosynthetic organic matter production, potentially offering an important 39 metabolic resource in the nutrient-limited deep-sea (Levin et al 2009, Dowell et al 2016. To 40 take advantage of this resource, fauna must overcome the environmental stress associated 41 with high-temperature, acidic and toxic conditions at SHVs (Levin et al 2013, Gollner et al 42 2015.…”

“…56 57 Biogeosciences Discuss., doi:10.5194/bg-2016Discuss., doi:10.5194/bg- -318, 2016 Manuscript under review for journal Biogeosciences with hydrothermal activity provides thermodynamic benefits and constraints to microbial 63 community assembly (Kallmeyer & Boetius 2004, Teske et al 2014) but also accelerates the 64 degradation of organic matter, giving rise to a wide variety of compounds, including 65 hydrocarbons and organic acids (Martens 1990, Whiticar & Suess 1990, Dowell et al 2016. 66Microbial aggregations are commonly visible on the sediment surface at SHVs (Levin et al 67 2009, Aquilina et al 2013, Sweetman et al 2013, Dowell et al 2016) but active communities 68 are distributed throughout the underlying sediment layers, occupying a wide range of 69 geochemical and thermal niches (reviewed by Teske et al 2014). Sedimented vents may 70 present several sources of organic matter to consumers (Bernardino et al 2012, Sweetman et 71 al.…”