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ORIGINAL ARTICLES

Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia

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Pages 537-550 | Received 06 May 2017, Accepted 25 Jun 2018, Published online: 03 Aug 2018

References

  • Bayer K, Kamke J, Hentschel U. 2014a. Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiology Ecology. 89:679–690. doi: 10.1111/1574-6941.12369
  • Bayer K, Moitinho-Silva L, Brümmer, F, Cannistraci CV, Ravasi T, Hentschel U. 2014b. GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiology Ecology. 90:832–843. doi: 10.1111/1574-6941.12441
  • Bell JJ. 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Science. 79:341–353. doi: 10.1016/j.ecss.2008.05.002
  • Blanquer A, Uriz MJ, Galand PE. 2013. Removing environmental sources of variation to gain insight on symbionts vs. transient microbes in high and low microbial abundance sponges. Environmental Microbiology. 15:3008–3019.
  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Reviews Microbiology. 6:245–252. doi: 10.1038/nrmicro1852
  • Brochier-Armanet C, Gribaldo S, Forterre P. 2012. Spotlight on the Thaumarchaeota. The ISME Journal. 6:227–230. doi: 10.1038/ismej.2011.145
  • Calcinai B, Bastari A, Bavestrello G, Bertolino M, Horcajadas SB, Pansini M, Makapedua DM, Cerrano C. 2017. Demosponge diversity from North Sulawesi, with the description of six new species. ZooKeys. 680:105–150. doi: 10.3897/zookeys.680.12135
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 7:335–336. doi: 10.1038/nmeth.f.303
  • Cebrian E, Uriz MJ, Garrabou J, Ballesteros E. 2011. Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS One. 6:e20211. doi: 10.1371/journal.pone.0020211
  • Chang C, Stewart RC. 1998. The two-component system regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiology. 117:723–731. doi: 10.1104/pp.117.3.723
  • Cleary DFR, Becking LE, de Voogd NJ, Pires ACC, Polónia ARM, Egas C, Gomes NCM. 2013. Habitat- and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiology Ecology. 85:465–482. doi: 10.1111/1574-6941.12135
  • de Goeij JM, Van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, Admiraal W. 2013. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science. 342:108–110. doi: 10.1126/science.1241981
  • de Voogd NJ, Cleary DFR. 2008. An analysis of sponge diversity and distribution at three taxonomic levels in the thousand islands/Jakarta Bay reef complex, West-Java, Indonesia. Marine Ecology. 29:205–215. doi: 10.1111/j.1439-0485.2008.00238.x
  • Diaz MC, Rützler K. 2001. Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science. 69:535–546.
  • Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods. 10:996–998. doi: 10.1038/nmeth.2604
  • Eggleston AK. 2007. DNA replication and repair. Nature. 447:923–923. doi: 10.1038/447923a
  • Erwin PM, Coma R, López-Sendino P, Serrano E, Ribes M, Olson J. 2015. Stable symbionts across the HMA-LMA dichotomy: low seasonal and interannual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiology Ecology. 91:fiv115. doi: 10.1093/femsec/fiv115
  • Erwin PM, Thacker RW. 2008. Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts. Molecular Ecology. 17:2937–2947. doi: 10.1111/j.1365-294X.2008.03808.x
  • Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T. 2012. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proceedings of the National Academy of Sciences. 109:E1878–E1887. doi: 10.1073/pnas.1203287109
  • Freeman CJ, Thacker RW. 2011. Complex interactions between marine sponges and their symbiotic microbial communities. Limnology and Oceanography. 56:1577–1586. doi: 10.4319/lo.2011.56.5.1577
  • Freeman CJ, Thacker RW, Baker DM, Fogel ML. 2013. Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? The ISME Journal. 7:1116–1125. doi: 10.1038/ismej.2013.7
  • Giles EC, Kamke J, Moitinho-Silva L, Taylor MW, Hentschel U, Ravasi T, Schmitt S. 2013. Bacterial community profiles in low microbial abundance sponges. FEMS Microbiology Ecology. 83:232–241. doi: 10.1111/j.1574-6941.2012.01467.x
  • Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR, Lindquist NL, Erpenbeck D, Wörheide G, Hentschel U. 2014. The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. The Biological Bulletin. 227:78–88. doi: 10.1086/BBLv227n1p78
  • Gomes NCM, Cleary DFR, Pinto FN, Egas C, Almeida A, Cunha A, Mendonça-Hagler LCS, Smalla K. 2010.Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLoS One. 5:e14065-a. doi: 10.1371/journal.pone.0014065
  • Gotelli NJ, Colwell RK. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters. 4:379–391. doi: 10.1046/j.1461-0248.2001.00230.x
  • Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe YI, Sugahara J, Preston C, de la Torre J, Richardson PM, DeLong EF. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proceedings of the National Academy of Sciences. 103:18296–18301. doi: 10.1073/pnas.0608549103
  • Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M. 2003. Microbial diversity of marine sponges. In: Sponges (Porifera). Berlin, Heidelberg: Springer; p. 59–88.
  • Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS. 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environmental Microbiology 68: 4431–4440. doi: 10.1128/AEM.68.9.4431-4440.2002
  • Hentschel U, Piel J, Degnan SM, Taylor MW. 2012. Genomic insights into the marine sponge microbiome. Nature Reviews Microbiology. 10:641–654. doi: 10.1038/nrmicro2839
  • Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schläppy M-L, Schleper C, Kuypers MMM. 2009. Complex nitrogen cycling in the sponge Geodia barretti. Environmental Microbiology. 11:2228–2243. doi: 10.1111/j.1462-2920.2009.01944.x
  • Holmes B, Blanch H. 2007. Genus-specific associations of marine sponges with Group I Crenarchaeotes. Marine Biology. 150:759–772. doi: 10.1007/s00227-006-0361-x
  • Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV. 2012. Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science. 335:587–590. doi: 10.1126/science.1212665
  • Jackson SA, Flemer B, McCann A, Kennedy J, Morrissey JP, O’Gara F, Dobson ADW, Virolle M-J. 2013. Archaea appear to dominate the microbiome of Inflatella pellicula deep sea sponges. PLoS One. 8:e84438. doi: 10.1371/journal.pone.0084438
  • Kamke J, Taylor MW, Schmitt S. 2010. Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. The ISME Journal. 4:498–508. doi: 10.1038/ismej.2009.143
  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 437:543–546. doi: 10.1038/nature03911
  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology. 31:814–821. doi: 10.1038/nbt.2676
  • Lee OO, Wang Y, Yang J, Lafi F, Al-Suwailem A, Qian P-Y. 2011. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. The ISME Journal. 5:650–664. doi: 10.1038/ismej.2010.165
  • Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T. 2012. Metaproteogenomic analysis of a community of sponge symbionts. The ISME Journal. 6:1515–1525. doi: 10.1038/ismej.2012.1
  • McMurray SE, Pawlik JR, Finelli CM. 2014. Trait-mediated ecosystem impacts: how morphology and size affect pumping rates of the Caribbean giant barrel sponge. Aquatic Biology. 23:1–13. doi: 10.3354/ab00612
  • Moitinho-Silva L, Seridi L, Ryu T, Voolstra CR, Ravasi T, Hentschel U. 2014. Revealing microbial functional activities in the Red Sea sponge Stylissa carteri by metatranscriptomics. Environmental Microbiology. 16:3683–3698. doi: 10.1111/1462-2920.12533
  • Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu YC, McCormack GP, López-Legentil S, Marchant R, Webster N, Thomas T, Hentschel U. 2017. Predicting the HMA-LMA status in marine sponges by machine learning. Frontiers in Microbiology. 8:32. doi: 10.3389/fmicb.2017.00752
  • Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Wagner H. 2009. Vegan: community ecology package. R Package Version. 1:15–14. http://www.cran.r-project.org/package=vegan
  • Oyserman BO, Moya F, Lawson CE, Garcia AL, Vogt M, Heffernen M, Noguera DR, McMahon KD. 2016a. Ancestral genome reconstruction identifies the evolutionary basis for trait acquisition in polyphosphate accumulating bacteria. The ISME Journal. 10:2931–2945. doi: 10.1038/ismej.2016.67
  • Oyserman BO, Noguera DR, del Rio TG, Tringe SG, McMahon KD. 2016b. Metatranscriptomic insights on gene expression and regulatory controls in candidatus Accumulibacter phosphatis. The ISME Journal. 10:810–822. doi: 10.1038/ismej.2015.155
  • Pires ACC, Cleary DFR, Almeida A, Cunha Â, Dealtry S, Mendonça-Hagler LCS, Smalla K, Gomes NCM. 2012. Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Applied and Environmental Microbiology. 78:5520–5528. doi: 10.1128/AEM.00386-12
  • Polónia ARM, Cleary DFR, Freitas R, Coelho, FJRC, de Voogd NJ, Gomes NCM. 2016. Comparison of archaeal and bacterial communities in two sponge species and seawater from an Indonesian coral reef environment. Marine Genomics. 29:69–80. doi: 10.1016/j.margen.2016.04.014
  • Polónia ARM, Cleary DFR, Freitas R, de Voogd NJ, Gomes NCM. 2015. The putative functional ecology and distribution of archaeal communities in sponges, sediment and seawater in a coral reef environment. Molecular Ecology. 24:409–423. doi: 10.1111/mec.13024
  • Polónia ARM, Cleary DFR, Freitas R, Gomes NCM, de Voogd NJ. 2017. Archaeal and bacterial communities of Xestospongia testudinaria and sediment differ in diversity, composition and predicted function in an Indonesian coral reef environment. Journal of Sea Research. 119:37–53. doi: 10.1016/j.seares.2016.10.007
  • Polónia ARM, Cleary DRF, Duarte LN, de Voogd NJ, Gomes NCM. 2014. Composition of archaea in seawater, sediment and sponges in the Kepulauan Seribu reef system, Indonesia. Microbial Ecology. 67:553–567. doi: 10.1007/s00248-013-0365-2
  • Preston CM, Wu KY, Molinski TF, DeLong EF. 1996. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proceedings of the National Academy of Sciences of the USA. 93:6241–6246. doi: 10.1073/pnas.93.13.6241
  • Ribes M, Dziallas C, Coma R, Riemann L. 2015. Microbial diversity and putative diazotrophy in high-and low-microbial-abundance Mediterranean sponges. Applied and Environmental Microbiology. 81:5683–5693. doi: 10.1128/AEM.01320-15
  • Ribes M, Jimenez E, Yahel G, Lopez-Sendino P, Diez B, Massana R, Sharp JH, Coma R. 2012. Functional convergence of microbes associated with temperate marine sponges. Environmental Microbiology. 14:1224–1239 doi: 10.1111/j.1462-2920.2012.02701.x
  • 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. doi: 10.1128/AEM.00878-08
  • Schmitt S, Wehrl M, Bayer K, Siegl A, Hentschel U. 2007. Marine sponges as models for commensal microbe–host interactions. Symbiosis. 44:43–50.
  • Schöttner S, Hoffmann F, Cárdenas P, Rapp HT, Boetius A, Ramette, A, Gilbert JA. 2013. Relationships between host phylogeny, host type and bacterial community diversity in cold-water coral reef sponges. PLoS One. 8:e55505. doi: 10.1371/journal.pone.0055505
  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology. 12:R60. doi: 10.1186/gb-2011-12-6-r60
  • Shannon E, Weaver W. 1949. The mathematical theory of communication. Urbana (IL): University of Illinois Press (125 pp).
  • Simpson TL. 1984. The Cell Biology of Sponges. New York: Springer-Verlag.
  • Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, Taylor MW. 2008. Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environmental Microbiology. 10:1087–1094. doi: 10.1111/j.1462-2920.2007.01515.x
  • Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD, Kjelleberg S. 2010. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. The ISME Journal. 4:1557–1567. doi: 10.1038/ismej.2010.74
  • Turque AS, Batista D, Silveira CB, Cardoso AM, Vieira RP, Moraes FC, Clementino MM, Albano RM, Paranhos R, Martins OB, et al. 2010. Environmental shaping of sponge associated archaeal communities. PLoS One. 5:e15774. doi: 10.1371/journal.pone.0015774
  • Webster NS, Taylor MW. 2012. Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology. 14:335–346. doi: 10.1111/j.1462-2920.2011.02460.x
  • Weisz JB, Hentschel U, Lindquist N, Martens CS. 2007. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Marine Biology. 152:475–483. doi: 10.1007/s00227-007-0708-y
  • Yahel G, Sharp JH, Marie D, Häse 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. Limnology and Oceanography. 48:141–149. doi: 10.4319/lo.2003.48.1.0141
  • Zhang CL, Xie W, Martin-Cuadrado AB, Rodriguez-Valera F. 2015. Marine group II archaea, potentially important players in the global ocean carbon cycle. Frontiers in Microbiology. 6:1–9.
  • Zhang F, Pita L, Erwin PM, Abaid S, López-Legentil S, Hill RT. 2014. Symbiotic archaea in marine sponges show stability and host specificity in community structure and ammonia oxidation functionality. FEMS Microbiology Ecology. 90:699–707. doi: 10.1111/1574-6941.12427

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