Abstract
Environmental conditions in hydrothermal vents are considered to be unsuitable for most marine organisms due to discharge of hot and acidic water with high sulfur content. The crab Xenograpsus testudinatus is endemic to the shallow-water hydrothermal vents of Kueishan Island, Taiwan. This study aimed to provide detailed information on the composition of eukaryotes and prokaryotes in the gut and stomach of X. testudinatus by using Illumina sequencing of the 16S and 18S ribosomal RNA genes. The mangrove crab Perisesarma bidens was also studied to compare the diet and gut microbial fauna of crabs from different habitats. X. testudinatus was found to feed on a wide array of organisms including algae, fishes, bivalves, copepods, and anthozoans, whereas P. bidens was found to feed mainly on Magnoliopsida plants. Soil bacteria such as Rodobacteraceae and cyanobacteria such as Oscillatoriphycidae were present in both crabs, but Mycoplasmataceae and Helicobacteraceae were found only in X. testudinatus. Our findings suggest that both X. testudinatus and P. bidens are scavengers feeding on both prokaryotes and eukaryotes. The results facilitate understanding of the feeding ecology of X. testudinatus and provide a database for the food web dynamics of shallow-water hydrothermal vents.
Similar content being viewed by others
References
Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574. doi:10.1890/12-2010.1
Andreote FD, Jiménez DJ, Chaves D et al (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One 7:e38600. doi:10.1371/journal.pone.0038600
Andreotti R, de León AAP, Dowd SE et al (2011) Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol 11:6. doi:10.1186/1471-2180-11-6
Barry JP, Buck KR, Kochevar RK et al (2002) Methane-based symbiosis in a mussel, Bathymodiolus platifrons, from cold seeps in Sagami Bay, Japan. Invertebr Biol 121:47–54
Bergquist DC, Eckner JT, Urcuyo IA et al (2007) Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web. Mar Ecol Prog Ser 330:49–65
Biebl H (2006) Hoeflea phototrophica sp. nov., a novel marine aerobic alphaproteobacterium that forms bacteriochlorophyll a. Int J Syst Evol Microbiol 56:821–826. doi:10.1099/ijs.0.63958-0
Blaser MJ (1997) Ecology of Helicobacter pylori in the human stomach. J Clin Invest 100:759–762. doi:10.1172/JCI119588
Bråte J, Logares R, Berney C et al (2010) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4:1144–1153. doi:10.1038/ismej.2010.39
Bright M, Eichinger I, von Salvini-Plawen L (2013) The metatrochophore of a deep-sea hydrothermal vent vestimentiferan (Polychaeta: Siboglinidae). Org Divers Evol 13:163–188
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303
Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522. doi:10.1073/pnas.1000080107
Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8
Cavanaugh CM, Gardiner SL, Jones ML et al (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342. doi:10.1126/science.213.4505.340
Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270
Chen C-TA, Wang B, Huang J et al (2005a) Investigation into extremely acidic hydrothermal fluids off Kueishan Tao, Taiwan, China. Acta Oceanol Sin 24:125–133
Chen C-TA, Zeng Z, Kuo F-W et al (2005b) Tide-influenced acidic hydrothermal system offshore NE Taiwan. Chem Geol 224:69–81. doi:10.1016/j.chemgeo.2005.07.022
Chen YJ, Wu JY, Chen CTA, Liu LL (2014) Effects of low pH stress on shell traits and proteomes of the dove snail, Anachis misera inhabiting shallow vent environments off Kueishan Islet, Taiwan. Biogeosci Discuss 11:17207–17226. doi:10.5194/bgd-11-17207-2014
Chen X, Di P, Wang H et al (2015) Bacterial community associated with the intestinal tract of Chinese mitten crab (Eriocheir sinensis) farmed in Lake Tai, China. PLoS One. doi:10.1371/journal.pone.0123990
Childress JJ, Fisher CR, Brooks JM et al (1986) A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233:1306–1308. doi:10.1126/science.233.4770.1306
Chow S, Suzuki S, Matsunaga T et al (2011) Investigation on natural diets of larval marine animals using peptide nucleic acid-directed polymerase chain reaction clamping. Mar Biotechnol 13:305–313. doi:10.1007/s10126-010-9301-3
Colwell RK, Chao A, Gotelli NJ et al (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21. doi:10.1093/jpe/rtr044
Comeault A, Stevens CJ, Juniper SK (2010) Mixed photosynthetic-chemosynthetic diets in vent obligate macroinvertebrates at shallow hydrothermal vents on Volcano 1, South Tonga Arc-Evidence from stable isotope and fatty acid analyses. Cah Biol Mar 51:351–359
Corbari L, Durand L, Cambon-Bonavita M-A et al (2012) New digestive symbiosis in the hydrothermal vent amphipoda Ventiella sulfuris. C R Biol 335:142–154. doi:10.1016/j.crvi.2011.12.005
Crawford PA, Crowley JR, Sambandam N et al (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci USA 106:11276–11281. doi:10.1073/pnas.0902366106
DeSantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. doi:10.1128/AEM.03006-05
Duperron S, Nadalig T, Caprais JC et al (2005) Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71:1694–1700. doi:10.1128/AEM.71.4.1694-1700.2005
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Fileman E, Lindeque P, Harmer R et al (2014) Feeding rates and prey selectivity of planktonic decapod larvae in the Western English Channel. Mar Biol 161:2479–2494
Fraune S, Zimmer M (2008) Host-specificity of environmentally transmitted mycoplasma-like isopod symbionts. Environ Microbiol 10:2497–2504
Gest H, Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136:11–16. doi:10.1007/BF00415602
Givens CE, Burnett KG, Burnett LE, Hollibaugh JT (2013) Microbial communities of the carapace, gut, and hemolymph of the Atlantic blue crab, Callinectes sapidus. Mar Biol 160:2841–2851. doi:10.1007/s00227-013-2275-8
Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264
Hata H, Tanabe AS, Yamamoto S et al (2014) Diet disparity among sympatric herbivorous cichlids in the same ecomorphs in Lake Tanganyika: amplicon pyrosequences on algal farms and stomach contents. BMC Biol 12:113. doi:10.1186/s12915-014-0090-4
Hoffman JA, Katz J, Bertness MD (1984) Fiddler crab deposit-feeding and meiofaunal abundance in salt marsh habitats. J Exp Mar Biol Ecol 82:161–174
Huang SF (1999) Marine algae of Kuei-San Dao. Taiwania 44:49–71
Hwang CY, Bae GD, Yih W, Cho BC (2009) Marivita cryptomonadis gen. nov., sp. nov. and Marivita litorea sp. nov., of the family Rhodobacteraceae, isolated from marine habitats. Int J Syst Evol Microbiol 59:1568–1575. doi:10.1099/ijs.0.005462-0
Hyde KD, Jones EBG, Liu J-K et al (2013) Families of Dothideomycetes. Fungal Divers 63:1–313. doi:10.1007/s13225-013-0263-4
Jeng M-S, Ng NK, Ng PKL (2004) Feeding behaviour: hydrothermal vent crabs feast on sea ‘snow’. Nature 432:969. doi:10.1038/432969a
Jiang X-T, Peng X, Deng G-H et al (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104. doi:10.1007/s00248-013-0238-8
Kharlamenko VI, Zhukova NV, Khotimchenko SV et al (1995) Fatty acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar Ecol Prog Ser 120:231–241. doi:10.3354/meps120231
Komai T, Chan TY (2010) A new genus and two new species of alvinocaridid shrimps (Crustacea: Decapoda: Caridea) from a hydrothermal vent field off northeastern Taiwan. Zootaxa 2372:15–32
Krick A, Kehraus S, Eberl L et al (2007) A marine Mesorhizobium sp. produces structurally novel long-chain N-acyl-L-homoserine lactones. Appl Environ Microbiol 73:3587–3594. doi:10.1128/AEM.02344-06
Lee SY (1998) Ecological role of grapsid crabs in mangrove ecosystems: a review. Mar Freshw Res 49:335–343
Lemaitre R (2004) Discovery of the first hermit crab (Crustacea: Decapoda: Parapaguridae) associated with hydrothermal vents. Cah Biol Mar 45:325–334
Levesque C, Limén H, Juniper SK (2005) Origin, composition and nutritional quality of particulate matter at deep-sea hydrothermal vents on Axial Volcano, NE Pacific. Mar Ecol Prog Ser 289:43–52. doi:10.3354/meps289043
Li K, Guan W, Wei G et al (2007) Phylogenetic analysis of intestinal bacteria in the Chinese mitten crab (Eriocheir sinensis). J Appl Microbiol 103:675–682
Lin F-J, Komai T, Chan T-Y (2007) A new species of callianassid shrimp (Crustacea: Decapoda: Thalassinidea) from deep-water hydrothermal vents off Taiwan. Proc Biol Soc Wash 120:143–158. doi:10.2988/0006-324X(2007)120[143:ANSOCS]2.0.CO;2
Lindeque P, Dimond A, Harmer R et al (2015) Feeding selectivity of bivalve larvae on natural plankton assemblages in the Western English Channel. Mar Biol 162:291–308
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. doi:10.1093/bioinformatics/btr507
McDonald D, Price MN, Goodrich J et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. doi:10.1038/ismej.2011.139
Meziti A, Mente E, Kormas KA (2012) Gut bacteria associated with different diets in reared Nephrops norvegicus. Syst Appl Microbiol 35:473–482. doi:10.1016/j.syapm.2012.07.004
Murdock S, Johnson H, Forget N, Juniper SK (2010) Composition and diversity of microbial mats at shallow hydrothermal vents on Volcano 1, South Tonga Arc. Cah Biol Mar 51:407–413
Ng NK, Davie P, Schubart CD, Ng PKL (2007) Xenograpsidae, a new family of grapsoid crabs (Crustacea: Brachyura) associated with shallow water hydrothermal vents. Raffles Bull Zool 16:233–256
O’Rorke R, Lavery S, Chow S et al (2012) Determining the diet of larvae of western rock lobster (Panulirus cygnus) using high-throughput DNA sequencing techniques. PLoS One 7:e42757. doi:10.1371/journal.pone.0042757
O’Rorke R, Lavery SD, Wang M et al (2014) Determining the diet of larvae of the red rock lobster (Jasus edwardsii) using high-throughput DNA sequencing techniques. Mar Biol 161:551–563. doi:10.1007/s00227-013-2357-7
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. ISME 7:96–109. doi:10.1038/ismej.2012.87
Poon DY, Chan BK, Williams GA (2010) Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) and Perisesarma bidens (Sesarmidae): implications for mangrove food webs. Hydrobiologia 638:29–40. doi:10.1007/s10750-009-0005-5
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. doi:10.1093/nar/gks1219
Spellerberg IF, Fedor PJ (2003) A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the “Shannon–Wiener”Index. Glob Ecol Biogeogr 12:177–179
Stachowicz JJ, Hay ME (1999) Reduced mobility is associated with compensatory feeding and increased diet breadth of marine crabs. Mar Ecol Prog Ser 188:169–178
Stein JL (1984) Subtidal gastropods consume sulfur-oxidizing bacteria: evidence from coastal hydrothermal vents. Science 223:696–698. doi:10.1126/science.223.4637.696
Stein JL, Cary SC, Hessler RR et al (1988) Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biol Bull 174:373–378
Takai K (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56:1725–1733. doi:10.1099/ijs.0.64255-0
Terahara T, Chow S, Kurogi H et al (2011) Efficiency of peptide nucleic acid-directed PCR clamping and its application in the investigation of natural diets of the Japanese eel leptocephali. PLoS One 6:e25715. doi:10.1371/journal.pone.0025715
Thimm T, Hoffmann A, Borkott H et al (1998) The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Appl Environ Microbiol 64:2660–2669
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. doi:10.1371/journal.pone.0026243
Vaidya B, Tanuku NRS, Pinnaka AK (2013) Albirhodobacter marinus gen. nov., sp. nov., a member of the family Rhodobacteraceae isolated from sea shore water of Visakhapatnam, India. Antonie Van Leeuwenhoek 103:347–355
Valverde A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989. doi:10.1099/ijs.0.63551-0
Van Dover CL, Fry B (1989) Stable isotopic compositions of hydrothermal vent organisms. Mar Biol 102:257–263. doi:10.1007/BF00428287
Vázquez-Baeza Y, Pirrung M, González A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. Giga Sci 2:16. doi:10.1186/2047-217X-2-16
Vestheim H, Deagle BE, Jarman SN (2011) Application of blocking oligonucleotides to improve signal-to-noise ratio in a PCR. Methods Mol Biol 687:265–274. doi:10.1007/978-1-60761-944-4_19
Wagner-Döbler I, Rheims H, Felske A et al (2003) Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea. Int J Syst Evol Microbiol 53:731–738
Wagner-Döbler I, Ballhausen B, Berger M et al (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. ISME J 4:61–77. doi:10.1038/ismej.2009.94
Wang Y, Stingl U, Anton-Erxleben F et al (2004) “Candidatus Hepatoplasma crinochetorum”, a new, stalk-forming lineage of Mollicutes colonizing the midgut glands of a terrestrial isopod. Appl Environ Microbiol 70:6166–6172. doi:10.1128/AEM.70.10.6166-6172.2004
Wang Z, Binder M, Hibbett DS (2005) Life history and systematics of the aquatic discomycete Mitrula (Helotiales, Ascomycota) based on cultural, morphological, and molecular studies. Am J Bot 92:1565–1574. doi:10.3732/ajb.92.9.1565
Wang Z, Binder M, Schoch CL et al (2006) Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): a nuclear rDNA phylogeny. Mol Phylogenet Evol 41:295–312. doi:10.1016/j.ympev.2006.05.031
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/AEM.00062-07
Wang T-W, Chan T-Y, Chan BKK (2014) Trophic relationships of hydrothermal vent and non-vent communities in the upper sublittoral and upper bathyal zones off Kueishan Island, Taiwan: a combined morphological, gut content analysis and stable isotope approach. Mar Biol 161:2447–2463. doi:10.1007/s00227-014-2479-6
Watsuji T-O, Yamamoto A, Motoki K et al (2015) Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri. ISME J 9:821–831. doi:10.1038/ismej.2014.178
Webb AP, Eyre BD (2004) The effect of natural populations of the burrowing and grazing soldier crab (Mictyris longicarpus) on sediment irrigation, benthic metabolism and nitrogen fluxes. J Exp Mar Biol Ecol 309:1–19. doi:10.1016/j.jembe.2004.05.003
Werry J, Lee SY (2005) Grapsid crabs mediate link between mangrove litter production and estuarine planktonic food chains. Mar Ecol Prog Ser 293:165–176
Wolcott TG (1984) Uptake of interstitial water from soil: mechanisms and ecological significance in the ghost crab Ocypode quadrata and two gecarcinid land crabs. Physiol Zool 57:161–184
Zarzoso-Lacoste D, Corse E, Vidal E (2012) Improving PCR detection of prey in molecular diet studies: importance of group-specific primer set selection and extraction protocol performances. Mol Ecol Resour 13:117–127. doi:10.1111/1755-0998.12029
Zbinden M, Cambon-Bonavita M-A (2003) Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Ecol 46:23–30. doi:10.1016/S0168-6496(03)00176-4
Zhang Y, Zhao Z, Chen C-TA et al (2012) Sulfur metabolizing microbes dominate microbial communities in andesite-hosted shallow-sea hydrothermal systems. PLoS One 7:e44593. doi:10.1371/journal.pone.0044593
Zimmer M, Danko J, Pennings S et al (2002) Cellulose digestion and phenol oxidation in coastal isopods (Crustacea: Isopoda). Mar Biol 140:1207–1213
Acknowledgments
We thank the students and technicians in the laboratories of CKW and JSH for their assistance. The work was supported by a Direct Grant for Research from The Chinese University of Hong Kong (Project no. 4053106 & 4053038) to CKW and a research grant from the Ministry of Science and Technology of Taiwan (MOST 104-2621-M-019-002) to JSH.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by O. Puebla.
Reviewed by undisclosed experts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Suppl. Figure 1
Principal coordinate analysis (PCoA) 2D plots of 18S rDNA libraries based on weighted, normalized UniFrac distance matrix. (a) PC1 vs PC2; (b) PC1 vs PC3; (c) PC2 vs PC3. MG (red) = gut content of Perisesarma bidens; MS (blue) = stomach content of P. bidens; NWG (orange) = gut content of Xenograpsus testudinatus captured in white vents in 2012; NWS (green) = stomach content of X. testudinatus captured in white vents in 2012; NYG (purple) = gut content of X. testudinatus captured in yellow vents in 2012; NYS (yellow) = stomach content of X. testudinatus captured in yellow vents in 2012; OWG (light blue) = gut content of X. testudinatus captured in white vents in 2011; OWS (pink) = stomach content of X. testudinatus captured in white vents in 2011. Percentages of total variation explained by each axis are shown in brackets (PPTX 273 kb)
Suppl. Figure 2
Principal coordinate analysis (PCoA) 2D plots of 16S rDNA libraries based on weighted, normalized UniFrac distance matrix. (a) PC1 vs PC2; (b) PC1 vs PC3; (c) PC2 vs PC3. MG (red) = gut content of Perisesarma bidens; MS (blue) = stomach content of P. bidens; NWG (orange) = gut content of Xenograpsus testudinatus captured in white vents in 2012; NWS (green) = stomach content of X. testudinatus captured in white vents in 2012; NYG (purple) = gut content of X. testudinatus captured in yellow vents in 2012; NYS (yellow) = stomach content of X. testudinatus captured in yellow vents in 2012; OWG (light blue) = gut content of X. testudinatus captured in white vents in 2011; OWS (pink) = stomach content of X. testudinatus captured in white vents in 2011. Percentages of total variation explained by each axis are shown in brackets (PPTX 272 kb)
Rights and permissions
About this article
Cite this article
Ho, T.W., Hwang, JS., Cheung, M.K. et al. Dietary analysis on the shallow-water hydrothermal vent crab Xenograpsus testudinatus using Illumina sequencing. Mar Biol 162, 1787–1798 (2015). https://doi.org/10.1007/s00227-015-2711-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-015-2711-z