全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Relationships between Host Phylogeny, Host Type and Bacterial Community Diversity in Cold-Water Coral Reef Sponges

DOI: 10.1371/journal.pone.0055505

Full-Text   Cite this paper   Add to My Lib

Abstract:

Cold-water coral reefs are known to locally enhance the diversity of deep-sea fauna as well as of microbes. Sponges are among the most diverse faunal groups in these ecosystems, and many of them host large abundances of microbes in their tissues. In this study, twelve sponge species from three cold-water coral reefs off Norway were investigated for the relationship between sponge phylogenetic classification (species and family level), as well as sponge type (high versus low microbial abundance), and the diversity of sponge-associated bacterial communities, taking also geographic location and water depth into account. Community analysis by Automated Ribosomal Intergenic Spacer Analysis (ARISA) showed that as many as 345 (79%) of the 437 different bacterial operational taxonomic units (OTUs) detected in the dataset were shared between sponges and sediments, while only 70 (16%) appeared purely sponge-associated. Furthermore, changes in bacterial community structure were significantly related to sponge species (63% of explained community variation), sponge family (52%) or sponge type (30%), whereas mesoscale geographic distances and water depth showed comparatively small effects (<5% each). In addition, a highly significant, positive relationship between bacterial community dissimilarity and sponge phylogenetic distance was observed within the ancient family of the Geodiidae. Overall, the high diversity of sponges in cold-water coral reefs, combined with the observed sponge-related variation in bacterial community structure, support the idea that sponges represent heterogeneous, yet structured microbial habitats that contribute significantly to enhancing bacterial diversity in deep-sea ecosystems.

References

[1]  Jensen A, Frederiksen R (1992) The fauna associated with the bank-forming deepwater coral Lophelia pertusa (Scleractinaria) on the Faroe Shelf. Sarsia 77: 53–69.
[2]  Freiwald A, Foss? JG, A, Koslow T, Roberts J (2004) Cold-water coral reefs. Cambridge: UNEP-WCMC. 86 p.
[3]  Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: The biology and geology of cold-water coral ecosystems. Science 312: 543–547.
[4]  Buhl-Mortensen L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, et al. (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar Ecol 31: 21–50.
[5]  Yakimov MM, Cappello S, Crisafi E, Tursi A, Savini A, et al. (2006) Phylogenetic survey of metabolically active microbial communities associated with the deep-sea coral Lophelia pertusa from the Apulian plateau, Central Mediterranean Sea. Deep Sea Res Part I Oceanogr Res Pap 53: 62–75.
[6]  Jensen S, Neufeld JD, Birkeland NK, Hovland M, Murrell JC (2008) Insights into the microbial community structure of a Norwegian deep-water coral reef environment. Deep-Sea Res I 55: 1554–1563.
[7]  Neulinger S, J?rnegren J, Ludvigsen M, Lochte K, Dullo W (2008) Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral's nutrition, health and distribution. Appl Environ Microbiol 74: 7272–7285.
[8]  Hanson L, Agis M, Maier C, Weinbauer M (2009) Community composition of bacteria associated with cold-water coral Madrepora oculata: within and between colony variability. Mar Ecol Prog Ser 397: 89–102.
[9]  Kellogg C, Lisle J, Galkiewicz J (2009) Culture-independent characterization of bacterial communities associated with the cold-water coral Lophelia pertusa in the Northeastern Gulf of Mexico. Appl Environ Microbiol 75: 2294–2303.
[10]  Sch?ttner S, Hoffmann F, Wild C, Rapp HT, Boetius A, et al. (2009) Inter- and intra-habitat bacterial diversity associated with cold-water corals. ISME J 3: 756–759.
[11]  Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, et al.. (2003) Microbial diversity of marine sponges. In: Müller WEG, editor. Marine Molecular Biotechnology. Berlin: Springer. pp. 59–88.
[12]  Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 259–347.
[13]  Webster N, Taylor M, Behnam F, Lucker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission of bacterial sponge symbionts. Environ Microbiol 12: 2070–2082.
[14]  Soest RWMv, Lavaleye MSS (2005) Diversity and abundance of sponges in bathyal coral reefs of Rockall Bank, NE Atlantic, from boxcore samples. Mar Biol Res 1: 338–349.
[15]  Schl?ppy M-L, Sch?ttner SI, Lavik G, Kuypers M, de Beer D, et al. (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157: 593–602.
[16]  Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, et al. (2005) An anaerobic world in sponges. Geomicrobiol J 22: 1–10.
[17]  Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, et al. (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11: 2228–2243.
[18]  Yahel G, Sharp JH, Marie D, Hase C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol Oceanogr 48: 141–149.
[19]  de Goeij JM, Moodley L, Houtekamer M, Carballeira NM, van Duyl FC (2008a) Tracing 13C-enriched dissolved and particulate organic carbon in Halisarca caerulea, a coral reef sponge with associated bacteria: evidence for DOM-feeding. Limnol Oceanogr 53: 1376–1386.
[20]  de Goeij JM, van Duyl FC (2007) Coral cavities are sinks of dissolved organic carbon (DOC). Limnol Oceanogr 52: 2608–2617.
[21]  de Goeij JM, van den Berg H, van Oostveen MM, Epping EHG, van Duyl FC (2008b) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357: 139–151.
[22]  Wild C, Mayr C, Sch?ttner S, Wehrmann L, Naumann M, et al. (2008) Organic matter release by cold water corals and its implication for fauna-microbe interaction. Mar Ecol Prog Ser 372: 67–75.
[23]  Weisz JB, Hentschel U, Lindquist N, Martens CS (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152: 475–483.
[24]  Weisz JB, Lindquist N, Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155: 367–376.
[25]  Kamke J, Taylor MW, Schmitt S (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs. 16S rRNA gene comparisons. ISME J 4: 498–508.
[26]  Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, et al. (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431–4440.
[27]  Simister RL, Deines P, Botté ES, Webster NS, Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Micobiol 14: 517–524.
[28]  Thoms C, Horn M, Wagner M, Hentschel U, Proksch P (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142: 685–692.
[29]  Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121–130.
[30]  Hill M, Hill A, Lopez N, Harriot O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148: 1221–1230.
[31]  Wichels A, Wurtz S, Dopke H, Schutt C, Gerdts G (2006) Bacterial diversity in the breadcrumb sponge Halichondria panicea (Pallas). FEMS Microbiol Ecol 56: 102–118.
[32]  Thiel V, Leininger S, Schmaljohann R, Brummer F, Imhoff JF (2007) Sponge-specific bacterial associations of the Mediterranean sponge Chondrilla nucula (Demospongiae, Tetractinomorpha). Microb Ecol 54: 101–111.
[33]  Lee OO, Wong YH, Qian P-Y (2009) Inter- and intra-specific variations of bacterial communities associated with marine sponges from San Juan Island, Washington, USS. Appl Environ Microbiol 75: 3513–3521.
[34]  Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 654–576.
[35]  Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14: 335–346.
[36]  Ereskovsky AV, Gonobobleva E, Vishnyakov A (2005) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146: 869–875.
[37]  Enticknap JJ, Kelly M, Peraud O, Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72: 3724–3732.
[38]  Schmitt S, Weisz JB, Lindquist N, Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73: 2067–2078.
[39]  Sharp K, Eam B, Faulkner D, Haygood M (2007) Vertical Transmission of Diverse Microbes in the Tropical Sponge Corticium sp. Appl Environ Microbiol 73: 622–629.
[40]  Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Applied and Environmental Microbiology 74: 7694–7708.
[41]  Erpenbeck D, Breeuwer AJ, van der Velde HC, Van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141: 377–386.
[42]  Thacker RW, Starnes S (2003) Host specificity of the symbiotic cyanobacterium Oscillatoria spongelia in marine sponges, Dysidea spp. Mar Biol 142: 643–648.
[43]  Holmes B, Blanch H (2007) Genus-specific associations of marine sponges with group I crenarchaeota. Mar Biol 150: 759–772.
[44]  Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10: 641–654.
[45]  Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65: 4630–4636.
[46]  Bienhold C, Boetius A, Ramette A (2012) The energy-diversity relationship of complex bacterial communities in Arctic deep-sea sediments. ISMEJ 6: 724–732.
[47]  Gobet A, B?er SI, Huse SM, van Beusekom JEE, Quince C, et al. (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISMEJ 6: 542–553.
[48]  Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, et al. (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Nat Acad Sci USA 103: 13104–13109.
[49]  Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A, et al. (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5: 650–664.
[50]  B?er S, Hedtkamp S, van Beusekom JEE, Fuhrman JA, Boetius A, et al. (2009) Time- and sediment depth-related variations of bacterial diversity and community structure in subtidal sands. ISME J 3: 780–791.
[51]  Brück WM, Brück TB, Self WT, Reed JK, Nitecki SS, et al. (2010) Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME J 4: 686–699.
[52]  Sch?ttner S, Pfitzner B, Grünke S, Rasheed M, Wild C, et al. (2011) Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environmental Microbiology 13: 1815–1826.
[53]  Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, et al. (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6: e24570.
[54]  Bent SJ, Forney LJ (2008) The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. The ISME Journal 2: 689–695.
[55]  Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495–2505.
[56]  Sch?ttner S, Wild C, Hoffmann F, Boetius A, Ramette A (2012) Spatial scales of bacterial diversity in cold-water coral reef ecosystems. PLoS ONE 7: e32093.
[57]  Cárdenas P, Pérez T, Boury-Esnault N (2012) Sponge systematics facing new challenges. Adv Mar Biol 61: 29–209.
[58]  Reitner J, Mehl D (1995) Early paleozoic diversification of sponges: new data and evidences. Geol Pal?ontol Mitt Innsbruck 20: 335–347.
[59]  Pisera A (2006) Paleontology of sponges – a review. Can J Zool 84: 242–261.
[60]  Sciscioli M, Scalera Liaci L, Lepore E, Gherardi M, Simpson TL (1991) Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (Porifera Demospongiae). Mol Reprod Dev 28: 346–350.
[61]  Sciscioli M, Lepore E, Gherardi M, Scalera Liaci L (1994) Transfer of symbiotic bacteria in the mature oocyte of Geodia cydonium (Porifera, Demospongiae): an ultrastructural study. Cah Biol Mar 35: 471–478.
[62]  Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218–230.
[63]  Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, et al. (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70: 6147–6156.
[64]  Cárdenas P, Xavier J, Tendal OS, Schander C, Rapp HT (2007) Redescription and resurrection of Pachymatisma normani (Demospongiae, Geodiidae), with remarks on the genus Pachymatisma. J Mar Biol Assoc UK 87: 1511–1525.
[65]  Cárdenas P, Rapp HT (2012) A review of Norwegian streptaster-bearing Astrophorida (Porifera: Demospongiae: Tetractinellida), new records and a new species. Zootaxa 3253: 1–53.
[66]  Cárdenas P, Xavier JR, Reveillaud J, Schander C, Rapp HT (2011) Molecular phylogeny of the Astrophorida (Porifera, Demospongiae) reveals an unexpected high level of spicule homoplasy. PLoS ONE 6: e18318.
[67]  Morrow CC, Picton BE, Erpenbeck D, Boury-Esnault N, Maggs CA, et al. (2012) Congruence between nuclear and mitochondrial genes in Demospongiae: A new hypothesis for relationships within the G4 clade (Porifera: Demospongiae). Mol Phylogenet Evol 62: 174–190.
[68]  Hooper JNA, van Soest RWM (2002) Systema Porifera. A guide to the classification of sponges. New York: Kluwer Academic/Plenum Publishers. 1708 pp.
[69]  Cárdenas P, Rapp HT, Schander C, Tendal OS (2010) Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) - combining phylogenetic and Linnaean classification. Zool Scr 39: 89–106.
[70]  Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142–160.
[71]  Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.
[72]  Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.
[73]  Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara R B, et al.. (2010) vegan: Community Ecology Package. R package version 1.17-4.
[74]  Nichols SA (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Mol Phylogenet Evol 34: 81–96.
[75]  Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol 26: 2261–2274.
[76]  Benjamin Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57: 289–300.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133