Evidence for the role of endosymbionts in PNAS PLUS regional-scale habitat partitioning by hydrothermal vent symbioses

Roxanne A. Beinarta, Jon G. Sandersa, Baptiste Faureb,c, Sean P. Sylvad, Raymond W. Leee, Erin L. Beckerb, Amy Gartmanf, George W. Luther IIIf, Jeffrey S. Seewaldd, Charles R. Fisherb, and Peter R. Girguisa,1 aDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138; bBiology Department, Pennsylvania State University, University Park, PA 16802; cInstitut de Recherche pour le Développement, Laboratoire d’Ecologie Marine, Université de la Réunion; 97715 Saint Denis de La Réunion, France; dDepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; eSchool of Biological Sciences, Washington State University, Pullman, WA 99164; and fSchool of Marine Science and Policy, University of Delaware, Lewes, DE 19958 AUTHOR SUMMARY

It is well-established that differ- reductants to harness energy ences in organisms’ intrinsic for inorganic carbon fixation, traits allow them to coexist by the primary source of carbon for using different habitats or both host and symbiont bio- resources, a phenomenon re- synthesis and growth (2). ferred to as “niche partitioning.” Conditions around vents are For symbiotic organisms, niche highly variable over space and partitioning has the potential to time, with geochemical and be influenced by the traits of physical gradients that provide both partners. Despite a growing a number of physiochemical appreciation for the ubiquity of niches at both local and re- microbe–animal and microbe– gional scales. plant symbioses in many envi- Results of previous studies ronments, studies linking of vent animals generally estab- microbial symbionts to patterns lish that certain species, in- of niche partitioning are sur- cluding some animal–microbial prisingly rare. Here, we present Fig. P1. The distribution of Alviniconcha snails along the regional- symbioses, are found in specific a comprehensive survey of a scale geochemical gradient at the ELSC corresponds to symbiont physical and chemical en- snail–microbial symbiosis at type. (A) A typical assemblage of Alviniconcha (Al) and other vent vironments, and many invoke deep-sea hydrothermal vents. animals in the Lau Basin (image courtesy of J. Childress, University of host physiological attributes, Snails of the genus Alviniconcha California, Santa Barbara, CA). (B) An individual Alviniconcha snail. such as tolerance of vent-fluid A B (C) Map of the ELSC, with four sampled vent fields shown across (Fig. P1 and ) are dominant the ∼300-km range. The wedges graphically represent the relative temperature and chemistry, as fauna at vents in the south Pa- driving these distributions. decrease in the concentrations of H2 and H2S in hydrothermal vent cific, clustering at high densities fluids from north to south. (D) The distribution of Alviniconcha However, it is equally likely that in areas with active hydrother- host types and dominant symbiont type across the ELSC. Snail host symbiont physiology influences mal venting. Alviniconcha host types (HT-I, HT-II, and HT-III) are indicated by the shape of each symbol. habitat utilization, but the chemoautotrophic bacteria, The dominant symbiont phylotypes [γ-proteobacteria type 1 (γ-1), role of the symbionts in this which fix carbon for both host γ-proteobacteria type Lau (γ-Lau), and ε-proteobacteria (ε)] within niche partitioning remains and symbiont biosynthesis and a host are indicated by the color of each symbol. largely unexplored. Here, we growth using energy generated characterized the relationships from the oxidation of vent-derived compounds (1). Our studies among symbiont type, host type, and geochemistry at hydro- revealed cryptic diversity in the host and symbionts, unrecognized thermal vents along ∼300 km of the Eastern Lau Spreading host–symbiont combinations (holobionts), and striking patterns of Center (ELSC) in the southwestern Pacific. Our survey ECOLOGY holobiont distribution across ∼300 km of an oceanic spreading of 288 Alviniconcha snails at four vent fields along the ELSC center (Fig. P1 C and D). Moreover, the distribution of symbiont uncovered three genetically distinct host types as well as three types corresponded to regional gradients in the concentrations of two vent-derived compounds (Fig. P1C) that can be used only by the symbionts, suggesting that Alviniconcha holobionts parti- ’ Author contributions: R.A.B., J.G.S., and P.R.G. designed research; R.A.B., J.G.S., B.F., A.G., tion their geochemical niches according to their symbionts and P.R.G. performed research; R.A.B., J.G.S., B.F., S.P.S., R.W.L., E.L.B., A.G., G.W.L., J.S.S., physiological capacity to use these compounds. These data rep- and C.R.F. analyzed data; and R.A.B. and P.R.G. wrote the paper. resent compelling evidence that niche partitioning by vent sym- The authors declare no conflict of interest. fl bioses might be in uenced by symbiont physiological capacity. This Direct Submission article had a prearranged editor. Hydrothermal vents are common in the ocean, found along Freely available online through the PNAS open access option. the midocean ridge system and tectonic margins. These vents fl Data deposition: The sequences reported in this paper have been deposited in the Gen- emit heated uids that are replete with reduced chemicals Bank database [accession nos. JN402310, JN402311, JQ624362–JQ624411 (Alviniconcha (reductants), such as hydrogen (H2) and hydrogen sulfide (H2S), spp. host mitochondrial CO1 sequences) and JN377487, JN377488, JN377489 (symbiont which are the end products of water–rock interactions at ele- 16S rRNA gene sequences)]. vated temperatures in the deep subsurface. Numerous vent 1To whom correspondence should be addressed. E-mail: [email protected]. invertebrates, like Alviniconcha, have evolved obligate symbiotic See full research article on page E3241 of www.pnas.org. relationships with intracellular bacteria that oxidize vent-derived Cite this Author Summary as: PNAS 10.1073/pnas.1202690109.

www.pnas.org/cgi/doi/10.1073/pnas.1202690109 PNAS | November 20, 2012 | vol. 109 | no. 47 | 19053–19054 Downloaded by guest on September 30, 2021 distinct symbiont types from two classes of the bacterial phylum oxidation of H2 and/or H2S, affects the regional distribution of Proteobacteria (one type from ε-proteobacteria and two from these symbioses. Future studies will ascertain the degree to γ-proteobacteria). We observed that each host type partnered which these compounds are used by the different symbionts. with a specific assemblage of symbionts; some host types These data illustrate the linkages that can exist between abi- associated with only one symbiont type, whereas others associ- otic and biological processes, because subsurface water–rock ated with multiple symbiont types. One particular host type interactions govern vent-fluid geochemistry, which in turn partnered with symbiont types from both bacterial classes, corresponds to regional-scale niche partitioning. These con- a rarity among vent animals hosting intracellular symbionts. nections provide a timely perspective on the role that symbionts Moreover, we observed a striking pattern in the prevalence likely play in governing faunal distribution at hydrothermal of the different host and symbiont associations (or holobionts) vents. Our increasing awareness of the prevalence of microbe– across the ELSC, wherein Alviniconcha host types with animal and microbe–plant interactions in many different ε-proteobacteria and γ-proteobacteria clearly dominated at the environments, both aquatic and terrestrial, indicates that the fi northern and southern vent elds, respectively (Fig. P1). This potential effect of microbial symbiont physiology on the – north south transition in symbiont type corresponded to large structure of other biological communities is likely significant. changes in the concentrations of H2 and H2S in the vent fluids, fl – which in turn result from changes in uid rock interaction in the 1. Suzuki Y, et al. (2006) Host-symbiont relationships in hydrothermal vent gastropods of deep subsurface (3). In situ measurements of sulfide within the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72(2): Alviniconcha habitats established that they are exposed to higher 1388–1393. 2. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: The art of H2S concentrations—and likely to higher H2 concentrations—at harnessing chemosynthesis. Nat Rev Microbiol 6(10):725–740. the northernmost vents. Because only the bacterial symbiont can 3. Bézos A, Escrig S, Langmuir CH, Michael PJ, Asimow PD (2009) Origins of chemical use these compounds for energy production, we posit that sym- diversity of back-arc basin basalts: A segment-scale study of the Eastern Lau Spreading biont physiology, specifically energy metabolism relating to the Center. Journal of Geophysical Reearch 114(B6):B06212, pp 1–25.

19054 | www.pnas.org/cgi/doi/10.1073/pnas.1202690109 Beinart et al. Downloaded by guest on September 30, 2021