title: Ontogenetic variation in epibiont community structure in the deep-sea yeti crab, Kiwa puravida: convergence among crustaceans.
abstract: Recent investigations have demonstrated that unusually 'hairy' yeti crabs within the family Kiwaidae associate with two predominant filamentous bacterial families, the Epsilon and Gammaproteobacteria. These analyses, however, were based on samples collected from a single body region, the setae of pereopods. To more thoroughly investigate the microbiome associated with Kiwa puravida, a yeti crab species from Costa Rica, we utilized barcoded 16S rRNA amplicon pyrosequencing, as well as microscopy and terminal restriction fragment length polymorphism analysis. Results indicate that, indeed, the bacterial community on the pereopods is far less diverse than on the rest of the body (Shannon indices ranged from 1.30-2.02 and 2.22-2.66, respectively). Similarly, the bacterial communities associated with juveniles and adults were more complex than previously recognized, with as many as 46 bacterial families represented. Ontogenetic differences in the microbial community, from egg to juvenile to adult, included a dramatic under-representation of the Helicobacteraceae and higher abundances of both Thiotrichaceae and Methylococcaceae for the eggs, which paralleled patterns observed in another bacteria-crustacean symbiosis. The degree to which abiotic and biotic feedbacks influence the bacterial community on the crabs is still not known, but predictions suggest that both the local environment and host-derived factors influence the establishment and maintenance of microbes associated with the surfaces of aquatic animals.
authors: Biology Department, Occidental College, Los Angeles, CA, 90041, USA.
authors: Shana K
authors: SK
authors: Goffredi
authors: Biology Department, Occidental College, Los Angeles, CA, 90041, USA.
authors: Ann
authors: A
authors: Gregory
authors: Environmental Genomics Core Facility, Environmental Health Sciences, University of South Carolina, Columbia, SC, 29208, USA.
authors: William J
authors: WJ
authors: Jones
authors: Biology Department, Occidental College, Los Angeles, CA, 90041, USA.
authors: Norma M
authors: NM
authors: Morella
authors: Biology Department, Occidental College, Los Angeles, CA, 90041, USA.
authors: Reid I
authors: RI
authors: Sakamoto
mesh_terms: D000818:Animals; D033381:Anomura / Q000382:microbiology*; D001419:Bacteria / Q000145:classification* / Q000235:genetics; D003364:Costa Rica; D058893:DNA Barcoding, Taxonomic; D005260:Female; D017404:In Situ Hybridization, Fluorescence; D064307:Microbiota; D046529:Microscopy, Electron, Transmission; D010063:Ovum / Q000382:microbiology; D010802:Phylogeny; D012150:Polymorphism, Restriction Fragment Length; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA; D013559:Symbiosis
chemical_list: D012336:RNA, Ribosomal, 16S
keywords: Kiwa; crab; deep-sea; epibiont; symbiosis
references: Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied and Environment Microbiology, 56, 1919-1925.
references: Becker K (1996) Epibionts on carapaces of some malacostracans from the Gulf of Thailand. Journal of Crustacean Biology, 16, 92-104.
references: Biagi E, Nylund L, Candela M et al. (2010) Through ageing, and beyond: gut micro- biota and inflammatory status in seniors and centenarians. PLoS ONE, 5, e10667.
references: Bulgheresi S, Schabussova I, Chen T, Mullin NP, Maizels RM, Ott JA. (2006) A new C-type lectin similar to the human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Applied and Environmental Microbiology, 72, 2950-2956.
references: Caporaso JG, Kuczynski J, Stombaugh J et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336.
references: Claesson MJ, Cusack S, O'Sullivan O et al. (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proceedings of the National Academy of Sciences of the United States of America, 108, 4586-4591.
references: Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial PRIMER-E Plymouth.
references: Corbari L, Zbinden M, Cambon-Bonavita MA, Gaill F, Compere P (2008) Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquatic Biology, 1, 225-238.
references: Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology, 22, 434-444.
references: Daniels CA, Zeifman A, Heym K et al. (2011) Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis. Marine Ecology Progress Series, 426, 29-40.
references: Dattagupta S, Schaperdoth I, Montanari A et al. (2009) A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. The ISME Journal, 3, 935-943.
references: Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature, 449, 811-818.
references: Dewhirst FE, Chen T, Izard J et al. (2010) The human oral microbiome. Journal of Bacteriology, 192, 5002-5017.
references: Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annual Review of Entomology, 49, 71-92.
references: Douglas AE (2009) The microbial dimension in insect nutritional ecology. Functional Ecology, 23, 38-47.
references: Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194-2200.
references: Franzenburg S, Fraune S, Altrock PM et al. (2013) Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. The ISME Journal, 7, 781-790.
references: Gill SR, Pop M, Deboy RT et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science, 312, 1355-1359.
references: Giribet G, Carranza S, Baguñà J, Riutort M, Ribera C (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution, 13, 76-84.
references: Goffredi SK (2010) Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environmental Microbiology Reports, 2, 479-488.
references: Goffredi SK, Waren A, Orphan VJ, Van Dover CL, Vrijenhoek RC (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Applied and Environment Microbiology, 70, 3082-3090.
references: Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC (2008) Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environmental Microbiology, 10, 2623-2634.
references: Grice EA, Segre JA (2012) The human microbiome: our second genome. Annual Review of Genomics and Human Genetics, 13, 151-170.
references: Grice EA, Kong HH, Conlan S et al. (2009) NISC Comparative Sequencing Program Topographical and temporal diversity of the human skin microbiome. Science, 324, 1190-1192.
references: Guri M, Durand L, Cueff-Gauchard V et al. (2012) Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. The ISME Journal, 6, 597-609.
references: Haddad A, Camacho F, Durand P, Cary SC (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Applied and Environment Microbiology, 61, 1679-1687.
references: Han X, Suess E, Sahling H, Wallmann K (2004) Fluid venting activity on the Costa Rica Margin: new results from authigenic carbonates. Geologische Rundschau, 93, 596-611.
references: Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nature Reviews Microbiology, 10, 641-654.
references: Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM (2011) Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS Biology, 6, e16018.
references: Human Microbiome Project Consortium (2012a) A framework for human microbiome research. Nature, 486, 215-221.
references: Human Microbiome Project Consortium (2012b) Structure, function and diversity of the healthy human microbiome. Nature, 486, 207-214.
references: Koenig JE, Spor A, Scalfone N et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 108, 4578-4585.
references: Li RW, Connor EE, Li C, Baldwin Vi RL, Sparks ME (2012) Characterization of the rumen microbiota of pre-ruminant calves using metagenomic tools. Environmental Microbiology, 14, 129-139.
references: Lin X, Wakeham SG, Putnam IF et al. (2006) Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Applied Environmental Microbiology, 72, 2679-2690.
references: Macpherson E, Jones W, Segonzac M (2005) A new squat lobster family of Galatheoidea (Crustacea, Decapoda, Anomura) from the hydrothermal vents of the Pacific-Antarctic Ridge. Zoosystema, 27, 709-723.
references: Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Systematic Applied Microbiology, 15, 593-600.
references: Miyake H, Kitada M, Tsuchida S, Okuyama Y, Nakamura K (2007) Ecological aspects of hydrothermal vent animals in captivity at atmospheric pressure. Marine Ecology, 28, 86-92.
references: Nussbaumer AD, Bright M, Baranyi C, Beisser CJ, Ott JA (2004) Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes. Aquatic Microbial Ecology, 34, 239-246.
references: Pernthaler A, Pernthaler J (2005) Simultaneous fluorescence in situ hybridization of mRNA and rRNA for the detection of gene expression in environmental microbes. Methods Enzymology, 397, 352-371.
references: Petersen JM, Ramette A, Lott C, Cambon-Bonavita MA, Zbinden M, Dubilier N (2009) Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environmental Microbiology, 12, 2204-2218.
references: Polz MF, Felbeck H, Novak R, Nebelsick M, Ott JA (1992) Chemoautotrophic, sulfur-oxidizing symbiotic bacteria on marine nematodes: morphological and biochemical characterization. Microbial Ecology, 24, 313-329.
references: Ponsard J, Cambon-Bonavita M-A, Zbinden M et al. (2013) Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. The ISME Journal, 7, 96-109.
references: Rogers AD, Tyler PA, Connelly DP et al. (2012) The discovery of new deep-sea hydrothermal vent communities in the southern ocean and implications for biogeography. PLoS Biology, 10, e1001234.
references: Shin SC, Kim S-H, You H et al. (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334, 670-674.
references: Steedman HF (1957) Polyester wax: a new ribboning embedding medium for histology. Nature, 179, 1345.
references: Suzuki Y, Suzuki M, Tsuchida S et al. (2009) Molecular investigations of the stalked barnacle Volcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand. Marine Biological Association of the UK, 89, 727-733.
references: Tanaka N, Romanenko LA, Lino T, Frolova GM, Mikhailov VV (2011) Cocleimonas flava gen nov, a gammaproteobacterium isolated from sand snail (Umbonium costatum). International Journal of Systematic and Evolutionary Microbiology, 61, 412-416.
references: Thurber AR, Jones WJ, Schnabel K (2011) Dancing for food in the Deep Sea: bacterial farming by a new species of yeti crab. PLoS ONE, 6, e26243.
references: Tsuchida S, Suzuki Y, Fujiwara Y et al. (2011) Epibiotic association between filamentous bacteria and the vent-associated galatheid crab, Shinkaia crosnieri (Decapoda: Anomura). Marine Biological Association of the UK, 91, 23-32.
references: Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA (1988) Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Marine Biology, 98, 209-216.
references: Watsuji T, Nakagawa S, Tsuchida S et al. (2010) Diversity and function of epibiotic microbial communities on the galatheid crab, Shinkaia crosnieri. Microbes Environment, 25, 288-294.
references: Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nature Reviews Genetics, 3, 850-861.
references: Zbinden M, Shillito B, Le Bris N et al. (2008) New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. Journal of Experimental Marine Biology and Ecology, 359, 131-140.