Diversity and abundance of ammonia-oxidizing Archaea and Bacteria in tropical and cold-water coral reef sponges

Aquatic Microbial Ecology

Volumn 68, Issue 3, 2013, Pages 215-230

  Cardoso, Joana F M F ^a,b   Van Bleijswijk, Judith D L ^a   Witte, Harry ^a   Van Duyl, Fleur C ^a  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

AmoA gene; Archaea; Bacteria; Marine; Sponges; Temperature

Indexed keywords

ANTHOZOA; ARCHAEA; BACTERIA (MICROORGANISMS); DEMOSPONGIAE; HALISARCA; HEXACTINELLIDA; HIGGINSIA;

EID: 84875391973     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01610     Document Type: Article

References (79)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
2. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925
3. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
4. Auguet JC, Nomokonova N, Camarero L, Casamayor EO (2011) Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oli-gotrophic alpine lakes. Appl Environ Microbiol 77: 1937-1945
5. 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
6. Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73: 5642-5647
7. Casamayor EO, Muyzer G, Pedrós Alió C (2001) Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA denaturing gradient gel electrophoresis and sequencing. Aquat Microb Ecol 25: 237-246
8. Cheng N, Fang Z, Huang H, Fang Z, Wu X, Bao S (2008) Phylogenetic diversity of bacteria and archaea associated with the marine sponge Pachychalina sp. Pol J Ecol 56: 505-510
9. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18: 117-143
10. Collin R, Díaz MC, Norenburg J, Rocha RM and others (2005) Photographic identification guide to some common marine invertebrates of Bocas Del Toro, Panama. Caribb J Sci 41: 638-707
11. Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33: 114-120
12. Daims H, Brühl 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
13. De Corte D, Yokokawa T, Varela MM, Agogué H, Herndl GJ (2009) Spatial distribution of Bacteria and Archaea and amoA gene copy numbers throughout the water column of the eastern Mediterranean Sea. ISME J 3: 147-158
14. De Goeij JM, Van den Berg H, Van Oostveen MM, Epping EHG, Van Duyl FC (2008) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357: 139-151
15. Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69: 535-546
16. Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156: 97-107
17. Diaz MC, Smith KP, Rützler K (2004) Sponge species richness and abundance as indicators of mangrove epibenthic community health. Atoll Res Bull 518: 1-11
18. Dohrmann M, Göcke C, Reed J, Janussen D (2012) Integrative taxonomy justifies a new genus, Nodastrella gen. nov., for North Atlantic 'Rossella' species (Porifera: Hexactinellida: Rossellidae). Zootaxa 3383: 1-13
19. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4: e95
20. Han M, Liu F, Zhang F, Li Z, Lin H (2012) Bacterial and archaeal symbionts in the South China Sea sponge Pha-kellia fusca: community structure, relative abundance, and ammonia-oxidizing populations. Mar Bio technol (NY) 14: 701-713
21. 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
22. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10: 641-654
23. Herfort L, Schouten S, Abbas B, Veldhuis MJW and others (2007) Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. FEMS Microbiol Ecol 62: 242-257
24. Hoffmann F, Radax R, Woebken D, Holtappels M and others (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11: 2228-2243
25. Holmes B, Blanch H (2007) Genus-specific associations of marine sponges with group I crenarchaeotes. Mar Biol 150: 759-772
26. Hooper JNA, Van Soest RWM (2002) Systema Porifera: a guide to the classification of Sponges. Kluwer Academic/Plenum Publishers, New York, NY
27. Hornek R, Pommerening-Röser A, Koops HP, Farnleiter AH, Kreuzinger N, Kirschner A, Mach RL (2006) Primers containing universal bases reduce multiple amoA gene specific DGGE band patterns when analysing the diversity of beta-ammonia oxidizers in the environment. J Microbiol Methods 66: 147-155
28. 2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem 267: 1534-1545
29. Jiménez E, Ribes M (2007) Sponges as a source of dissolved inorganic nitrogen: nitrification mediated by temperate sponges. Limnol Oceanogr 52: 948-958
30. Kalanetra KM, Bano N, Hollibaugh JT (2009) Ammonia-oxidizing Archaea in the Arctic Ocean and Antarctic coastal waters. Environ Microbiol 11: 2434-2445
31. Klotz MG, Alzerreca JJ, Norton JM (1997) A gene encoding a membrane protein exists upstream of the amoA/amoB genes in ammonia-oxidizing bacteria; a third member of the amo operon? FEMS Microbiol Lett 150: 65-73
32. Kobluk DR, Van Soest RWM(1989) Cavity-dwelling sponges in a southern Caribbean coral reef and their paleontological implications. Bull Mar Sci 44: 1207-1235
33. 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
34. Liu F, Han M, Zhang F, Zhang B, Li Z (2011) Distribution and abundance of archaea in South China Sea sponge Holoxea sp. and the presence of ammonia-oxidizing Archaea in sponge cells. Evid Based Complement Alternat Med 2011: 723696
35. Llirós M, Casamayor EO, Borrego CM (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol Ecol 66: 331-342
36. López-Legentil S, Erwin PM, Pawlik JR, Song B (2010) Effects of sponge bleaching on ammonia-oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Microb Ecol 60: 561-571
37. Ludwig W, Strunk O, Westram R, Richter L and others (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371
38. Margot H, Acebal C, Toril E, Amils R, Fernández JL (2002) Consistent association of crenarchaeal Archaea with sponges of genus Axinella. Mar Biol 140: 739-745
39. McTavish H, Fuchs JA, Hooper AB (1993) Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol 175: 2436-2444
40. Meyer B, Kuever J (2008) Phylogenetic diversity and spatial distribution of the microbial community associated with the Caribbean deep-water sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA gene analysis. Microb Ecol 56: 306-321
41. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9: 1162-1175
42. Mohamed NM, Enticknap JJ, Lohr JE, McIntosh SM, Hill RT (2008) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol 74: 1209-1222
43. 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
44. Montalvo NF, Hill RT (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microbiol 77: 7207-7216
45. Norton JM, Alzerreca JJ, Suwa Y, Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch Microbiol 177: 139-149
46. O'Mullan GD, Ward BB (2005) Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California. Appl Environ Microbiol 71: 697-705
47. Pape T, Hoffmann F, Queric NV, Von Juterzenka K, Reitner J, Michaelis W (2006) Dense populations of Archaea associated with the demosponge Tentorium semisuberites Schmidt, 1870 from Arctic deep-waters. Polar Biol 29: 662-667
48. Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68: 3094-3101
49. Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14: 300-306
50. Preston CM, Wu KY, Molinski TF, Delong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93: 6241-6246
51. Radax R, Hoffmann F, Rapp HT, Leininger S, Schleper C (2012) Ammonia-oxidizing archaea as main drivers of nitrification in cold water sponges. Environ Microbiol 14: 909-923
52. Reitner J, Hoffmann F (2003) Porifera-Zonierungen in Kaltwasser- Korallenriffen (Sula-Rücken, Norwegen). In: Gradstein SR, Willmann R, Zizka G (eds) Biodiversitätsforschung: die Entschlüsselung der Artenvielfalt in Raum und Zeit. Kleine Senckenberg-Reihe 45, Schwei-zerbart'sche Verlagsbuchhandlung, Stuttgart
53. Ribes M, Jiménez E, Yahel G, López-Sendino P and others (2012) Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol 14: 1224-1239
54. Sahan E, Muyzer G (2008) Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol Ecol 64: 175-186
55. Scheffers SR, Nieuwland G, Bak RPM, Van Duyl FC (2004) Removal of bacteria and nutrient dynamics within the coral reef framework of Curaçao (Netherlands Antilles). Coral Reefs 23: 413-422
56. Schläppy 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
57. Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10: 2979-2990
58. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14: 517-524
59. Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr 53: 986-996
60. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690
61. 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. Environ Microbiol 10: 1087-1094
62. Taylor MW, Radax R, Steger D, Wagner M (2007) Spongeassociated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347
63. Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ (2004) Combining catalyzed reporter deposition? fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Appl Environ Microbiol 70: 4411-4414
64. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10: 1357-1364
65. Turque AS, Cardoso AM, Silveira CB, Vieira RP and others (2008) Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de Janeiro, Brazil. Mar Biol 155: 135-146
66. Turque AS, Batista D, Silveira CB, Cardoso AM and others (2010) Environmental shaping of sponge-associated archaeal communities. PLoS ONE 5: e15774
67. Vacelet J, Donadey C (1987) A new species of Halisarca (Porifera, Demospongiae) from the Caribbean with remarks on the cytology and affinities of the genus. In: Jones WC (ed) European contribution to the taxonomy of sponges. Litho Press, Midleton
68. Van Duyl FC, Scheffers SR, Thomas IM, Driscoll M (2006) The effect of water exchange on bacterioplankton depletion and inorganic nutrient dynamics in coral reef cavities. Coral Reefs 25: 23-36
69. Van Duyl FC, Hegeman J, Hoogstraten A, Maier C (2008) Dissolved carbon fixation by sponge-microbe consortia of deep water coral mounds in the northeastern Atlantic Ocean. Mar Ecol Prog Ser 358: 137-150
70. Van Soest RWM (1978) Marine sponges from Curacao and other Caribbean localities: Keratosa. Foundation for Scientific Research in Surinam and The Netherlands Antilles, Utrecht
71. Van Soest RWM, Cleary DFR, De Kluijver MJ, Lavaleye MSS, Maier C, Van Duyl FC (2007a) Sponge diversity and community composition in Irish bathyal coral reefs. Contrib Zool 76: 121-142
72. Van Soest RWM, Van Duyl FC, Maier C, Lavaleye MSS, Beglinger EJ, Tabachnick KR (2007b) Mass occurrence of Rossella nodastrella Topsent on bathyal coral reefs of Rockall Bank, W of Ireland (Lyssacinosida, Hexactinellida). In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G (eds) Trends in Porifera research-biodiversity, innovation and sustainability. Proc 7th Int Sponge Conf, Buzios 6-13 May 2006, Brazil, p 645-652
73. Van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K and others (2012) World Porifera database. Available at: www.marinespecies.org/porifera/
74. Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136-143
75. Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14: 335-346
76. Webster NS, Watts JEM, Hill RT (2001) Detection and phylogenetic analysis of novel crenarchaeote and eury-archaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol (NY) 3: 600-608
77. Webster NS, Taylor MW, Behnam F, Lücker S and others (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082
78. Wuchter C, Abbas B, Coolen MJ, Herfort L and others (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103: 12317-12322
79. Yang J, Sun J, Lee OO, Wong YH, Qian PY (2011) Phylogenetic diversity and community structure of sponge-associated bacteria from mangroves of the Caribbean Sea. Aquat Microb Ecol 62: 231-240