Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges

FEMS Microbiology Ecology

Volumn 78, Issue 3, 2011, Pages 497-510

  Schmitt, Susanne ^a,b   Deines, Peter ^b   Behnam, Faris ^c   Wagner, Michael ^c   Taylor, Michael W ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

Bacterial symbionts; Chloroflexi; Phylogenetic diversity; Sponges

Indexed keywords

BACTERIAL DNA; RNA 16S; SEA WATER;

ABUNDANCE; BACTERIUM; CORAL; GENETIC ANALYSIS; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; PHYLOGENETICS; SEAWATER; SPECIES DIVERSITY; SPONGE; SYMBIONT; TAXONOMY;

ANIMAL; ARTICLE; BACTERIUM IDENTIFICATION; BIODIVERSITY; CHLOROFLEXI; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; NEW ZEALAND; PHYLOGENY; SPONGE (PORIFERA);

ANIMALS; BACTERIAL TYPING TECHNIQUES; BIODIVERSITY; CHLOROFLEXI; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, BACTERIAL; GENE LIBRARY; IN SITU HYBRIDIZATION, FLUORESCENCE; NEW ZEALAND; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEAWATER;

NEW ZEALAND;

ANTHOZOA; BACTERIA (MICROORGANISMS); CHLOROFLEXI; CHLOROFLEXI (CLASS);

EID: 81155125194     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01179.x     Document Type: Article

References (63)

1. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Amann RI, Krumholz L & Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental-studies in microbiology. J Bacteriol 172: 762-770.
3. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ & Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71: 7724-7736.
4. Bayer K, Schmitt S & Hentschel U (2008) Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ Microbiol 10: 2942-2955.
5. Bjornsson L, Hugenholtz P, Tyson GW & Blackall LL (2002) Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal. Microbiology 148: 2309-2318.
6. Blunt JW, Copp BR, Munro MHG, Northcote PT & Prinsep MR (2010) Marine natural products. Nat Prod Rep 27: 165-237.
7. Bruck WM, Bruck TB, Self WT, Reed JK, Nitecki SS & McCarthy PJ (2010) Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME J 4: 686-699.
8. Cassler M, Peterson CL, Ledger A, Pomponi SA, Wright AE, Winegar R, McCarthy PJ & Lopez JV (2008) Use of real-time qPCR to quantify members of the unculturable heterotrophic bacterial community in a deep sea marine sponge, Vetulina sp. Microb Ecol 55: 384-394.
9. Daims H, Bruhl A, Amann R, Schleifer KH & 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. Syst Appl Microbiol 22: 434-444.
10. Ehrlich H, Simon P, Carrillo-Cabrera W et al. (2010) Insights into chemistry of biological materials: newly discovered silica-aragonite-chitin biocomposites in demosponges. Chem Mater 22: 1462-1471.
11. 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.
12. Fieseler L, Horn M, Wagner M & Hentschel U (2004) Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl Environ Microbiol 70: 3724-3732.
13. Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P & Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134: 461-470.
14. Friedrich AB, Fischer I, Proksch P, Hacker J & Hentschel U (2001) Temporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38: 105-113.
15. Gauthier MEA, Du Pasquier L & Degnan BM (2010) The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and interleukin 1 receptor pathways. Evol Dev 12: 519-533.
16. Gich F, Garcia-Gil J & Overmann J (2001) Previously unknown and phylogenetically diverse members of the green nonsulfur bacteria are indigenous to freshwater lakes. Arch Microbiol 177: 1-10.
17. Grozdanov L & Hentschel U (2007) An environmental genomics perspective on the diversity and function of marine sponge-associated microbiota. Curr Opin Microbiol 10: 215-220.
18. 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. Appl Environ Microbiol 68: 4431-4440.
19. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J & Horn M (2003) Microbial diversity of marine sponges. Marine Molecular Biotechnology, (Mueller W, ed.), pp. 59-88. Springer, Berlin.
20. Hochmuth T, Niederkruger H, Gernert C, Siegl A, Taudien S, Platzer M, Crews P, Hentschel U & Piel J (2010) Linking chemical and microbial diversity in marine sponges: possible role for Poribacteria as producers of methyl-branched fatty acids. Chembiochem 11: 2572-2578.
21. Hoffmann F, Rapp HT & Reitner J (2006) Monitoring microbial community composition by fluorescence in situ hybridization during cultivation of the marine cold-water sponge Geodia barretti. Mar Biotechnol (NY) 8: 373-379.
22. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schlaeppy M-L, Schleper C & Kuypers MMM (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11: 2228-2243.
23. Hugenholtz P, Goebel BM & Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765-7447.
24. Jackson DJ, Macis L, Reitner J, Degnan BM & Worheide G (2007) Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science 316: 1893-1895.
25. Juretschko S, Timmermann G, Schmid MC, Schleifer KH, Pommerening-Roser A, Koops HP & Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64: 3042-3051.
26. 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.
27. Kennedy J, Marchesi JR & Dobson ADW (2007) Metagenomic approaches to exploit the biotechnological potential of the microbial consortia of marine sponges. Appl Microbiol Biotechnol 75: 11-20.
28. Lafi FF, Fuerst JA, Fieseler L, Engels C, Goh WWL & Hentschel U (2009) Widespread distribution of Poribacteria in Demospongiae. Appl Environ Microbiol 75: 5695-5699.
29. Laport MS, Santos OCS & Muricy G (2009) Marine sponges: potential sources of new antimicrobial drugs. Curr Pharm Biotechnol 10: 86-105.
30. Lozupone C, Hamady M & Knight R (2006) UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7: 371.
31. Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, Bachleitner M & Schleifer KH (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19: 554-568.
32. Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
33. Maldonado M (2007) Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types. J Mar Biol Assoc UK 87: 1701-1713.
34. Mohamed NM, Rao V, Hamann MT, Kelly M & Hill RT (2008a) Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microbiol 74: 4133-4143.
35. Mohamed NM, Enticknap JJ, Lohr JE, McIntosh SM & Hill RT (2008b) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol 74: 1209-1222.
36. Mohamed NM, Saito K, Tal Y & Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4: 38-48.
37. Noyer C, Hamilton A, Sacristan-Soriano O & Becerro MA (2010) Quantitative comparison of bacterial communities in two Mediterranean sponges. Symbiosis 51: 239-243.
38. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J & Gloeckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
39. Reiswig HM (1981) Partial carbon and energy budgets of the bacteriosponge Verongia fistularis (Porifera: Demospongiae) in Barbados West-Indies. Mar Ecol 2: 273-294.
40. Schlappy ML, Schottner SI, Lavik G, Kuypers MMM, de Beer D & Hoffmann F (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157: 593-602.
41. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl EnvironMicrobiol 75: 7537-7541.
42. Schmitt S, Wehrl M, Lindquist N, Weisz JB & Hentschel U (2007a) Morphological and molecular analyses of microorganisms in Caribbean reef adult sponges and in corresponding reproductive material. Porifera Research: Biodiversity, Innovation & Sustainability. (Custodio M, Lobo-Hajdu G, Hajdu E & Muricy G, eds), pp. 561-568. Rio de Janeiro Museu Nacional, Buzios, Brazil.
43. Schmitt S, Weisz JB, Lindquist N & Hentschel U (2007b) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73: 2067-2078.
44. 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. Appl Environ Microbiol 74: 7694-7708.
45. Schmitt S, Tsai P & Bell J et al. (2011) Assessing the complex sponge microbiota - core, variable, and species-specific bacterial communities in marine sponges. ISME J, in press.
46. Siegl A & Hentschel U (2010) PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ Microbiol Rep 2: 507-513.
47. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T & Hentschel U (2011) Singel-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5: 61-70.
48. Sipkema D, Holmes B, Nichols SA & Blanch HW (2009) Biological characterisation of Haliclona (?gellius) sp.: sponge and associated microorganisms. Microb Ecol 58: 903-920.
49. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM & Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored "rare biosphere". P Natl Acad Sci USA 103: 12115-12120.
50. 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.
51. Taylor MW, Radax R, Steger D & Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
52. 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.
53. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD & Kjelleberg S (2010a) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4: 1557-1567.
54. Thomas TRA, Kavlekar DP & LokaBharathi PA (2010b) Marine drugs from sponge-microbe association - a review. Mar Drugs 8: 1417-1468.
55. Vogel G (2008) The inner lives of sponges. Science 320: 1028-1030.
56. Webster NS & Blackall LL (2009) What do we really know about sponge-microbial symbioses? ISME J 3: 1-3.
57. Webster NS, Cobb RE & Negri AP (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2: 830-842.
58. Webster NS, Taylor MW, 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. Environ Microbiol 12: 2070-2082.
59. 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.
60. Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S & Muller WEG (2007) Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol Biol Evol 24: 792-804.
61. Wilkinson CR (1979) Nutrient translocation from symbiotic cyanobacteria to coral reef sponges. Biologie des spongiaires, (Levi C & BouryEsnault N, eds), pp. 373-380. Colloques International du Centre National de la Recherche Scientifique, Paris, France.
62. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H & Kamagata Y (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56: 1331-1340.
63. Zhu P, Li QZ & Wang GY (2008) Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microb Ecol 55: 406-414.