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Alvinella Pompejana Is an Endemic Inhabitant Tof Deep-Sea Hydrothermal Vents Located from 21°N to 32°S Latitude on the East Pacific Rise (1)

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Alvinella Pompejana Is an Endemic Inhabitant Tof Deep-Sea Hydrothermal Vents Located from 21°N to 32°S Latitude on the East Pacific Rise (1) Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility Joseph J. Grzymskia,1, Alison E. Murraya,1, Barbara J. Campbellb, Mihailo Kaplarevicc, Guang R. Gaoc,d, Charles Leee, Roy Daniele, Amir Ghadirif, Robert A. Feldmanf, and Stephen C. Caryb,d,2 aDivision of Earth and Ecosystem Sciences, Desert Research Institute, 2215 Raggio Parkway, Reno, NV 89512; bCollege of Marine and Earth Studies, University of Delaware, Lewes, DE 19958; cDelaware Biotechnology Institute, 15 Innovation Way, Newark, DE 19702; dElectrical and Computer Engineering, University of Delaware, 140 Evans Hall, Newark, DE 19716; eDepartment of Biological Sciences, University of Waikato, Hamilton, New Zealand; fSymBio Corporation, 1455 Adams Drive, Menlo Park, CA 94025 Edited by George N. Somero, Stanford University, Pacific Grove, CA, and approved September 17, 2008 (received for review March 20, 2008) Hydrothermal vent ecosystems support diverse life forms, many of the thermal tolerance of a structural protein biomarker (5) which rely on symbiotic associations to perform functions integral supports the assertion that A. pompejana is likely among the to survival in these extreme physicochemical environments. Epsi- most thermotolerant and eurythermal metazoans on Earth lonproteobacteria, found free-living and in intimate associations (6, 7). with vent invertebrates, are the predominant vent-associated A. pompejana is characterized by a filamentous microflora that microorganisms. The vent-associated polychaete worm, Alvinella forms cohesive hair-like projections from mucous glands lining pompejana, is host to a visibly dense fleece of episymbionts on its the polychaete’s dorsal intersegmentary spaces (8). The episym- dorsal surface. The episymbionts are a multispecies consortium of biont community is constrained to the bacterial subdivision, Epsilonproteobacteria present as a biofilm. We unraveled details of Epsilonproteobacteria, (9)—a taxonomic class that is widely these enigmatic, uncultivated episymbionts using environmental represented in hydrothermal vent ecosystems on surfaces, free- genome sequencing. They harbor wide-ranging adaptive traits living, in symbioses with invertebrates, in sediments and the that include high levels of strain variability analogous to Epsilon- shallow subsurface (10, 11). Distribution of the 2 dominant proteobacteria pathogens such as Helicobacter pylori, metabolic members (5A and 13B) of this Epsilonproteobacteria consortium diversity of free-living bacteria, and numerous orthologs of pro- (9) appears highly structured along each hair-like projection. teins that we hypothesize are each optimally adapted to specific The community was reported to comprise between 10 to 15 temperature ranges within the 10–65 °C fluctuations characteristic phylotypes (related at Ն99% SSU rRNA gene identity), of which of the A. pompejana habitat. This strategic combination enables Ͼ98% were Epsilonproteobacteria (9). Most described host- the consortium to thrive under diverse thermal and chemical symbiont associations consist of either monospecific relation- regimes. The episymbionts are metabolically tuned for growth in ships [e.g., Euprymna squid–Vibrio fischeri (12)] or more often, hydrothermal vent ecosystems with genes encoding the complete divergent multispecies associations [e.g., termites (13), marine rTCA cycle, sulfur oxidation, and denitrification; in addition, the oligochaete, Olavius algarvensis (14)]. However, population-level episymbiont metagenome also encodes capacity for heterotrophic variation has been observed in some symbioses, such as the and aerobic metabolisms. Analysis of the environmental genome marine sponge Axinella mexicana, which is associated with 2 suggests that A. pompejana may benefit from the episymbionts dominant crenarchaeotal populations (15) and the gammapro- serving as a stable source of food and vitamins. The success of teobacterial endosymbionts of the vent tubeworm Riftia pachy- Epsilonproteobacteria as episymbionts in hydrothermal vent eco- ptila (16). The diverse yet phylogenetically constrained episym- systems is a product of adaptive capabilities, broad metabolic bionts of A. pompejana are in stark contrast to a vent-associated capacity, strain variance, and virulent traits in common with shrimp from the Mid-Atlantic Ridge, Rimicaris exoculata, which pathogens. has established a more conventional single-species association with an epsilonproteobacterium (11). Although the A. pompe- Epsilonproteobacteria ͉ hydrothermal vent jana episymbionts have eluded isolation, molecular approaches have revealed that two of the dominant epsilonproteobacterial phylotypes have the capability for chemolithoautotrophic growth he polychaete Alvinella pompejana is an endemic inhabitant Tof deep-sea hydrothermal vents located from 21°N to 32°S latitude on the East Pacific Rise (1). This tube-dwelling Author contributions: A.E.M., B.J.C., G.R.G., R.D., R.A.F., and S.C.C. designed research; B.J.C. polychaete forms dense colonies exclusively on the walls of and A.G. performed research; J.J.G., A.E.M., B.J.C., M.K., C.L., and S.C.C. analyzed data; and high-temperature black smoker chimneys (2, 3), which are J.J.G., A.E.M., B.J.C., and S.C.C. wrote the paper. characterized by extreme physicochemical gradients and dy- The authors declare no conflict of interest. namic in thermal emission rates and intensive mineral precipi- This article is a PNAS Direct Submission. tation. The high-temperature diffuse flow surrounding the Freely available online through the PNAS open access option. worms’ tubes is acidic (pH 4.2–6.1) carrying high levels of total Data deposition: The Whole Genome Shotgun project has been deposited in the DDBJ/ (free ϩ complexed) hydrogen sulfide (Ͼ1 mM), ammonia EMBL/GenBank database (accession no. AAUQ00000000); the version described in this (3.8–10 ␮m), and reactive heavy metals (0.3–200 ␮M) including paper is the first version (accession no. AAUQ01000000). The project is registered with ␮ project ID 17241 and consists of sequences AAUQ01000001–AAUQ01128934. Traces were ferrous iron (290–840 m) (2). Temperature fluctuations in the submitted to the National Center for Biotechnology Information Trace Archive (accession actual tubes of A. pompejana range from 29 °C to 84 °C while the nos. 1878413299–1878706363); PCR-amplified SSU rRNA gene sequences were also sub- chemical conditions are anoxic, slightly acidic to near neutral pH mitted (accession nos. EF462586–EF462837). (5.33–6.9), and rich in electron acceptors (sulfate, nitrate, Fe III, 1J.J.G. and A.E.M. contributed equally to this work. and Mg) as well as potentially lethal levels of heavy metals (2, 3). 2To whom correspondence should be addressed. E-mail: [email protected]. The tube fluids contain surprisingly low levels of free H2S(Ͻ0.2 This article contains supporting information online at www.pnas.org/cgi/content/full/ ␮M to 46.53 ␮M) and are a mix of ambient seawater (72–91%) 0802782105/DCSupplemental. supplemented with vent-derived emissions (3, 4). An analysis of © 2008 by The National Academy of Sciences of the USA 17516–17521 ͉ PNAS ͉ November 11, 2008 ͉ vol. 105 ͉ no. 45 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802782105 Downloaded by guest on September 30, 2021 0.09 0.08 m r 0.07 J R E M 0.06 j e 0.05 S C l c 0.04 ho L P HO N s 0.03 t I GF p 0.02 f g U K V ki Pathogen or Free-living Cog usage Cog or Free-living Pathogen v T 0.01 DQu Fig. 1. Rarefaction curves for SSU rRNA genes and selected proteins in the dqn EM. Rarefaction curves were determined for the SSU rRNA gene (216 bases, 79 0 Bb 0 0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.08 0.09 sequences at 99% similarity) and the following proteins: recombinase subunit EM-C Cog usage A (recA, 280 bases, 43 sequences at 99% similarity), DNA gyrase subunit B (gyrB, 239 bases, 34 sequences at 99% similarity), heat shock protein 60 (groEL, Fig. 2. COG distributions in the EM-C dataset compared with 3 pathogenic 167 bases, 34 sequences at 98% similarity), ribosomal protein S12 (rpS12, 233 epsilonproteobacteria (bold, capitalized letters) and 3 free-living bacteria bases, 28 sequences at 99% similarity), and malate dehydrogenase (mdh, 263 (lowercase letters). The letters indicate the specific COG role category. bases, 20 sequences at 99% similarity). coding genes (Fig. 1) identified between 6 and 31 distinct via the reductive TCA cycle (17). Until recently, it was believed sequences, respectively. carbon was solely fixed chemoautotrophically via the Calvin The EM dataset consisted of 300,607 high-quality reads that Benson cycle in vent microbial communities (17). assembled into short contigs at 95% nucleotide identity (Table We performed an environmental genomic analysis of the A. S2). Attempts to bin either the raw sequence data or the pompejana episymbiont community in an effort to define the assembled data based on GϩC content were unsuccessful be- basic metabolic strategy of the association and elucidate why cause the data were almost uniformly distributed around the Epsilonproteobacteria are so successful in this environment. We 35% average (Fig. S4). The assembled contigs averaged 1,462 bp hypothesized that under extreme constraints imposed by the in length and comprised 38.5 MB. The total dataset (68 MB), local geochemical environment, the Epsilonproteobacteria epi- including singletons, contained 128,412 sequences. A total of symbiotic consortium employs a core metabolic strategy shared 103,371 proteins was predicted from these data. Forty-one by most members of
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