In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 109, No. 47 ( 2012-11-20)
Abstract:
These data illustrate the linkages that can exist between abiotic and biological processes, because subsurface water–rock interactions govern vent-fluid geochemistry, which in turn corresponds to regional-scale niche partitioning. These connections provide a timely perspective on the role that symbionts likely play in governing faunal distribution at hydrothermal vents. Our increasing awareness of the prevalence of microbe–animal and microbe–plant interactions in many different environments, both aquatic and terrestrial, indicates that the potential effect of microbial symbiont physiology on the structure of other biological communities is likely significant. Moreover, we observed a striking pattern in the prevalence of the different host and symbiont associations (or holobionts) across the ELSC, wherein Alviniconcha host types with ε-proteobacteria and γ-proteobacteria clearly dominated at the northern and southern vent fields, respectively ( Fig. P1 ). This north–south transition in symbiont type corresponded to large changes in the concentrations of H 2 and H 2 S in the vent fluids, which in turn result from changes in fluid–rock interaction in the deep subsurface ( 3 ). In situ measurements of sulfide within Alviniconcha habitats established that they are exposed to higher H 2 S concentrations—and likely to higher H 2 concentrations—at the northernmost vents. Because only the bacterial symbiont can use these compounds for energy production, we posit that symbiont physiology, specifically energy metabolism relating to the oxidation of H 2 and/or H 2 S, affects the regional distribution of these symbioses. Future studies will ascertain the degree to which these compounds are used by the different symbionts. Results of previous studies of vent animals generally establish that certain species, including some animal–microbial symbioses, are found in specific physical and chemical environments, and many invoke host physiological attributes, such as tolerance of vent-fluid temperature and chemistry, as driving these distributions. However, it is equally likely that symbiont physiology influences habitat utilization, but the role of the symbionts in this niche partitioning remains largely unexplored. Here, we characterized the relationships among symbiont type, host type, and geochemistry at hydrothermal vents along ∼300 km of the Eastern Lau Spreading Center (ELSC) in the southwestern Pacific. Our survey of 288 Alviniconcha snails at four vent fields along the ELSC uncovered three genetically distinct host types as well as three distinct symbiont types from two classes of the bacterial phylum Proteobacteria (one type from ε-proteobacteria and two from γ-proteobacteria). We observed that each host type partnered with a specific assemblage of symbionts; some host types associated with only one symbiont type, whereas others associated with multiple symbiont types. One particular host type partnered with symbiont types from both bacterial classes, a rarity among vent animals hosting intracellular symbionts. Hydrothermal vents are common in the ocean, found along the midocean ridge system and tectonic margins. These vents emit heated fluids that are replete with reduced chemicals (reductants), such as hydrogen (H 2 ) and hydrogen sulfide (H 2 S), which are the end products of water–rock interactions at elevated temperatures in the deep subsurface. Numerous vent invertebrates, like Alviniconcha , have evolved obligate symbiotic relationships with intracellular bacteria that oxidize vent-derived reductants to harness energy for inorganic carbon fixation, the primary source of carbon for both host and symbiont biosynthesis and growth ( 2 ). Conditions around vents are highly variable over space and time, with geochemical and physical gradients that provide a number of physiochemical niches at both local and regional scales. It is well-established that differences in organisms’ intrinsic traits allow them to coexist by using different habitats or resources, a phenomenon referred to as “niche partitioning.” For symbiotic organisms, niche partitioning has the potential to be influenced by the traits of both partners. Despite a growing appreciation for the ubiquity of microbe–animal and microbe–plant symbioses in many environments, studies linking microbial symbionts to patterns of niche partitioning are surprisingly rare. Here, we present a comprehensive survey of a snail–microbial symbiosis at deep-sea hydrothermal vents. Snails of the genus Alviniconcha ( Fig. P1 A and B ) are dominant fauna at vents in the south Pacific, clustering at high densities in areas with active hydrothermal venting. Alviniconcha host chemoautotrophic bacteria, which fix carbon for both host and symbiont biosynthesis and growth using energy generated from the oxidation of vent-derived compounds ( 1 ). Our studies revealed cryptic diversity in the host and symbionts, unrecognized host–symbiont combinations (holobionts), and striking patterns of holobiont distribution across ∼300 km of an oceanic spreading center ( Fig. P1 C and D ). Moreover, the distribution of symbiont types corresponded to regional gradients in the concentrations of two vent-derived compounds ( Fig. P1 C ) that can be used only by the symbionts, suggesting that Alviniconcha holobionts partition their geochemical niches according to their symbionts’ physiological capacity to use these compounds. These data represent compelling evidence that niche partitioning by vent symbioses might be influenced by symbiont physiological capacity.
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1202690109
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2012
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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