Microbial biofilms associated with fluid chemistry and megafaunal colonization at post-eruptive deep-sea hydrothermal vents

Abstract

At deep-sea hydrothermal vents, reduced, super-heated hydrothermal fluids mix with cold, oxygenated seawater. This creates temperature and chemical gradients that support chemosynthetic primary production and a biomass-rich community of invertebrates. In late 2005/early 2006 an eruption occurred on the East Pacific Rise at 9°50′N, 104°17′W. Direct observations of the post-eruptive diffuse-flow vents indicated that the earliest colonizers were microbial biofilms. Two cruises in 2006 and 2007 allowed us to monitor and sample the early steps of ecosystem recovery. The main objective of this work was to characterize the composition of microbial biofilms in relation to the temperature and chemistry of the hydrothermal fluids and the observed patterns of megafaunal colonization. The area selected for this study had local seafloor habitats of active diffuse flow (in-flow) interrupted by adjacent habitats with no apparent expulsion of hydrothermal fluids (no-flow). The in-flow habitats were characterized by higher temperatures (1.6–25.2 °C) and H₂S concentrations (up to 67.3 µM) than the no-flow habitats, and the microbial biofilms were dominated by chemosynthetic Epsilonproteobacteria. The no-flow habitats had much lower temperatures (1.2–5.2 °C) and H₂S concentrations (0.3–2.9 µM), and Gammaproteobacteria dominated the biofilms. Siboglinid tubeworms colonized only in-flow habitats, while they were absent at the no-flow areas, suggesting a correlation between siboglinid tubeworm colonization, active hydrothermal flow, and the composition of chemosynthetic microbial biofilms.

Introduction

Studies of diffuse-flow hydrothermal vents at 9°50′N on the East Pacific Rise (hereafter referred to as EPR) following seafloor volcanic eruptions (in 1991 and 2006) have provided information about processes controlling the initial colonization by microbial biofilms and subsequent succession of vent metazoans (Shank et al., 1998, Govenar, 2012, Sievert and Vetriani, 2012). While, in general, metazoan colonization correlates with temperature and hydrothermal fluid chemistry (Shank et al., 1998, Luther et al., 2001, Luther et al., 2012), biological interactions may also play a role in colonization patterns (e.g., Mullineaux et al., 2003; Govenar et al., 2012). Many vent invertebrates rely on chemosynthetic microorganisms that convert the energy of the reduced chemical species dissolved in the hydrothermal fluids into biochemical energy (ATP) to fix carbon dioxide. Also, in other marine habitats, microbial cues of metazoan settlement are critically important. Dispersive larvae respond not only to the texture and composition of microorganisms in biofilms, but also to chemicals produced by microbial consortia or individual microbial species (reviewed by Underwood and Keough, 2001, Hadfield, 2011). In addition, metamorphosis from the free-swimming larval stage to the sessile adult stage can be initiated by a different composition of the biofilms (Tebben et al., 2011, Yang et al., 2013).

Hence, chemosynthetic microorganisms may provide useful cues that indicate habitat quality for metazoan colonizers. Indeed, biologists have long hypothesized that microbial biofilms at deep-sea hydrothermal vents may interact with vent larvae to induce settlement and metamorphosis (Van Dover, 2000, Adams et al., 2012). However, this hypothesis remains largely untested.

Direct observation of the colonization of diffuse-flow vents following a volcanic eruption on the EPR has shown that microbial biofilms are the pioneer colonizers of newly-formed vents (Lutz et al., 2001, Sievert and Vetriani, 2012). Further, small subunit rRNA gene surveys of vent microbial communities indicated that Epsilonproteobacteria were the dominant microorganisms associated with the colonization of substrates, as well as the most abundant primary producers at diffuse-flow hydrothermal vents (Lopez-Garcia et al., 2003, Alain et al., 2004, Campbell et al., 2006, Sievert and Vetriani, 2012).

In December 2003, we initiated colonization studies at diffuse-flow vents located on the EPR to examine the correlation between microbial and megafaunal colonizers. In late 2005/early 2006, a volcanic seafloor eruption buried many of the pre-existing benthic communities in fresh lava (Cowen et al., 2007). The eruption also created more than 20 nascent vent habitats, establishing a time-zero for subsequent biological colonization and community development. While previous studies have documented post-eruptive changes in the chemistry of diffuse-vent fluids (Shank et al., 1998, Von Damm and Lilley, 2004), an integrated investigation that simultaneously examined the structure of early microbial colonists, megafaunal colonization and fluid chemistry in diffuse-flow vents had not been conducted.

Here we conducted time-series in situ experiments to examine patterns of microbial community structure and composition, fluid temperature and chemistry and megafaunal colonization at various post-eruptive diffuse-flow vents on the EPR. The goal of this study was to examine for the first time co-located linkages between hydrothermal fluid chemistry, microbial biofilms and megafaunal colonization. Specifically, amongst newly-formed, post-eruptive vents, we aimed to: (1) characterize the composition of microbial colonizers; (2) correlate patterns of microbial colonization in response to different geochemical regimes; and (3) examine patterns of megafaunal colonization. Our findings revealed marked differences in the composition of microbial biofilms and vent-endemic megafaunal colonization at hydrothermally active (in-flow) and inactive (no-flow) areas.