Sponge heterotrophic capacity and bacterial community structure in high- and low-microbial abundance sponges

Marine Ecology

Volumn 35, Issue 4, 2014, Pages 414-424

  Poppell, Ericka ^a,c   Weisz, Jeremy ^b   Spicer, Lori ^a   Massaro, Andrew ^a,d   Hill, April ^a   Hill, Malcolm ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b LINFIELD COLLEGE   (United States)

^c HAWAII PACIFIC UNIVERSITY   (United States)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

Bacteria; Choanocytes; Sponge; Symbiosis

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 84916894440     PISSN: 01739565     EISSN: 14390485     Source Type: Journal    
DOI: 10.1111/maec.12098     Document Type: Article

References (47)

1. Bouxin G. (2005) Ginkgo, a multivariate analysis package. Journal of Vegetation Science, 16, 355-359.
2. Conway K.W., Krautter M., Barrie J.V., Neuweiller M. (2001) Hexactinellid sponge reefs on the Canadian continental shelf: a unique 'living fossil'. Geoscience Canada, 28, 71-78.
3. De Goeij J.M., De Kluijver A., Van Duyl F.C., Vacelet J., Wijffels R.H., De Goeij A.F.P.M., Cleutjens J.P.M., Schutte B. (2009) Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding. Journal of Experimental Marine Biology and Ecology, 212, 3892-3900.
4. Diaz M.C., Ward B.B. (1997) Sponge-mediated nitrification in tropical benthic communities. Marine Ecology Progress Series, 156, 97-107.
5. Enticknap J.J., Thompson R., Peraud O., Lohr J.E., Hamann M.T., Hill R.T. (2004) Molecular analysis of a Florida Keys sponge: implications for natural products discovery. Marine Biotechnology, 6, 288-293.
6. Gerçe B., Schwartz T., Syldatk C., Hausmann R. (2011) Differences between bacterial communities associated with the surface or tissue of Mediterranean sponge species. Microbial Ecology, 61, 769-782.
7. Giles E.C., Kamke J., Moitinho-Silva L., Taylor M.W., Hentschel U., Ravasi T., Schmitt S. (2013) Bacterial community profiles in low microbial abundance sponges. FEMS Microbiology Ecology, 83, 232-241.
8. Hentschel U., Usher K.M., Taylor M.W. (2006) Marine sponges as microbial fermenters. FEMS Microbiology Ecology, 55, 167-77.
9. Hill M., Hill A., Lopez N., Harriott O. (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Marine Biology, 148, 1221-1230.
10. Isaacs L.T., Kan J., Nguyen L., Videau P., Anderson M.A., Wright T.L., Hill R.T. (2009) Comparison of the bacterial communities of wild and captive sponge Clathria prolifera from the Chesapeake Bay. Marine Biotechnology, 11, 758-770.
11. Johnson I.S., Hildemann W.H. (1982) Cellular organization in the marine demosponge Callyspongia diffusa. Marine Biology, 67, 1-7.
12. Lynch T.C., Philips E.J. (2000) Filtration of the bloom-forming cyanobacteria Synechococcus by three sponge species from Florida Bay, USA. Bulletin of Marine Science, 67, 923-1213.
13. Magurran A.E. (1988) Ecological Diversity and its Measurement. Princeton University Press, Princeton: 179 pp.
14. Massaro A.J., Weisz J.B., Hill M.S., Webster N.S. (2012) Behavioral and morphological changes caused by thermal stress in the Great Barrier Reef sponge Rhopaloeides odorabile. Journal of Experimental Marine Biology and Ecology, 416-417, 5, 5-60.
15. Muyzer G., Schafer H. (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Methods in Microbiology, 30, 425-468.
16. Nikolcheva L.G., Bärlocher F. (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycological Progress, 3, 41-49.
17. Palumbi S.R. (1984) Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science, 225, 1478-1480.
18. Peterson B., Fry B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18, 293-320.
19. Ribes M., Coma R., Gili J.M. (1999) Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Marine Ecology Progress Series, 176, 179-190.
20. Richardson C., Hill M., Marks C., Runyen-Janecky L., Hill A. (2012) Experimental manipulation of sponge/bacterial symbiont community composition with antibiotics: sponge cell aggregates as a unique tool to study animal/microorganism symbiosis. FEMS Microbiology Ecology, 81, 407-418.
21. Schlappy M.L., Schottner G.L., Kuypers M.M., Beer D., Hoffman F. (2010) Evidence of nitrification and denitrification in high and low microbial abundant sponges. Marine Biology, 157, 593-602.
22. Schmitt S., Weisz J.B., Lindquist N., Hentschel U. (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Applied Environmental Microbiology, 73, 2067.
23. Schmitt S., Tsai P., Bell J., Fromont J., Ilan M., Linquist N., Perez T., Rodrigo A., Schupp P.J., Vacelet J., Webster N., Hentschel U., Taylor M.W. (2011) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME Journal, 6, 564-576.
24. Schneider C.A., Rasband W.S., Eliceiri K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
25. Southwell M.W. (2007) Sponge impacts on coral reef nitrogen cycling, Key Largo, Florida. Ph.D. thesis, University of North Carolina at Chapel Hill.
26. Southwell M.W., Popp B.N., Martens C.S. (2007) Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Marine Chemistry, 108, 96-108.
27. Southwell M.W., Popp B.N., Martens C.S. (2008a) Nitrification controls in fluxes and isotopic composition of nitrate from Florida Keys sponges. Marine Chemistry, 108, 96-108.
28. Southwell M.W., Weisz J.B., Martens C.S., Lindquist N. (2008b) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnology Oceanography, 53, 986-996.
29. Taylor M.W., Hill R.T., Piel J., Thacker R.W., Hentschel U. (2007a) Soaking it up: the complex lives of marine sponges and their microbial associates. ISME Journal, 1, 187-190.
30. Taylor M.W., Radax R., Steger D., Wagner M. (2007b) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews, 71, 295-347.
31. Treonis A.M., Austin E.A., Buyer J.S., Maul J.E., Spicer L., Zasada A.I. (2010) Effects of organic amendment and tillage on soil microorganisms and microfauna. Applied Soil Ecology, 46, 103-110.
32. Vacelet J., Donadey C. (1977) Electron microscope study of the association between some sponges and bacteria. Journal of Experimental Marine Ecology, 30, 301-314.
33. Vogel S. (1978) Evidence for one-way valves in water-flow system of sponges. Journal of Experimental Biology, 76, 137-148.
34. Von Wintzingerode F., Gobel U.B., Stackebrandt E. (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiology Reviews, 21, 213-229.
35. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into new bacterial taxonomy. Applied Environmental Microbiology, 73, 5261-5267.
36. Webster N.S., Taylor M.W. (2012) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology, 14, 335-346.
37. Webster N.S., Taylor M.W., Behnam F., Luecker S., Rattei T., Whalan S., Horn M., Wagner M. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology, 12, 2070-2082.
38. Wehrl M. (2001) Untersuchungen zur Interaktion des marinen Schwammes Aplysina aerophoba mit assoziierten Mikroorganismen. Masters thesis, Universität Würzburg, Würzburg, Germany.
39. Weisz J. (2006) Measuring impacts of associated microbial communities on Caribbean reef sponges: searching for symbiosis. Ph.D. thesis, University of North Carolina at Chapel Hill.
40. Weisz J., Hentschel U., Lindquist N., Martens C. (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Marine Biology, 152, 475-483.
41. Weisz J.B., Lindquist N., Martens C.S. (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologica, 155, 367-376.
42. Weisz J.B., Massaro A.J., Ramsby B.D., Hill M.S. (2010) Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biological Bulletin, 219, 189-197.
43. West B., Brandt J., Holstien K., Hill A., Hill M. (2009) Fern-associated arbuscular mycorrhizal fungi are represented by multiple Glomus spp.: do environmental factors influence partner identity? Mycorrhiza, 19, 295-304.
44. White J.R., Patel J., Ottesen A., Arce G., Blackwelder P., Lopez J.V. (2012) Pyrosequencing of bacterial symbionts within Axinella corrugata sponges: diversity and seasonal variability. PLoS ONE, 7, e38204.
45. Wilkinson C.R. (1978) Microbial associations in sponges I. Ecology, physiology and microbial populations of coral reef sponges. Marine Biology, 49, 161-167.
46. Yahel G., Sharp J.H., Marie D., Hase C., Genin A. (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: bulk DOC in the major source for carbon. Limnology Oceanography, 48, 141-149.
47. Zar J.H. (2004) Biostatistical Analysis, 5th edn. Prentice-Hall, Inc., New York: 906 pp.