Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea

Molecular Ecology

Volumn 23, Issue 6, 2014, Pages 1348-1363

  Moitinho Silva, Lucas ^a   Bayer, Kristina ^a   Cannistraci, Carlo V ^b   Giles, Emily C ^b   Ryu, Taewoo ^b   Seridi, Loqmane ^b   Ravasi, Timothy ^b   Hentschel, Ute ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

marine sponges; microbial diversity; pyrosequencing; sponge specific microbes; symbiosis; transcriptional activity

Indexed keywords

BACTERIA (MICROORGANISMS); CANDIDATUS PORIBACTERIA; NITROSPIRA; OTUS; PROTEOBACTERIA; STYLISSA CARTERI; XESTOSPONGIA;

BACTERIAL DNA; RNA 16S; SEA WATER;

ANIMAL; ARTICLE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; GENETIC TRANSCRIPTION; GENETICS; INDIAN OCEAN; MARINE SPONGES; MICROBIAL DIVERSITY; MICROBIOLOGY; MICROFLORA; PHYLOGENY; PYROSEQUENCING; SPECIES DIFFERENCE; SPONGE (PORIFERA); SPONGE-SPECIFIC MICROBES; SYMBIOSIS; TRANSCRIPTIONAL ACTIVITY;

MARINE SPONGES; MICROBIAL DIVERSITY; PYROSEQUENCING; SPONGE-SPECIFIC MICROBES; SYMBIOSIS; TRANSCRIPTIONAL ACTIVITY;

ANIMALS; BACTERIA; BIODIVERSITY; DNA, BACTERIAL; INDIAN OCEAN; MICROBIOTA; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84896363836     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12365     Document Type: Article

References (64)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. Angermeier H, Kamke J, Abdelmohsen UR, et al,. (2011) The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microbiology Ecology, 75, 218-230.
3. Arellano SM, Lee OO, Lafi FF, et al,. (2013) Deep Sequencing of Myxilla (Ectyomyxilla) methanophila, an epibiotic sponge on cold-seep tubeworms, reveals methylotrophic, thiotrophic, and putative hydrocarbon-degrading microbial associations. Microbial Ecology, 65, 450-461.
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. Environmental Microbiology, 10, 2942-2955.
5. Bray JR, Curtis JT, (1957) An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs, 27, 325-349.
6. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL, (2011) Activity of abundant and rare bacteria in a coastal ocean. Proceedings of the National Academy of Sciences of the United States of America, 108, 12776-12781.
7. Cannistraci CV, Ravasi T, Montevecchi FM, Ideker T, Alessio M, (2010) Nonlinear dimension reduction and clustering by Minimum Curvilinearity unfold neuropathic pain and tissue embryological classes. Bioinformatics, 26, i531-i539.
8. Caporaso JG, Bittinger K, Bushman FD, et al,. (2010a) PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics, 26, 266-267.
9. Caporaso JG, Kuczynski J, Stombaugh J, et al,. (2010b) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336.
10. Chao A, (1984) Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270.
11. Chao A, Lee S-M, (1992) Estimating the number of classes via sample coverage. Journal of the American Statistical Association, 87, 210-217.
12. Colwell RK, (2009) Biodiversity: concepts, patterns, and measurement. In: The Princeton Guide to Ecology (ed, Levin SA,), pp. 257-263. Princeton Univ. Press, Princeton, New Jersey.
13. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460-2461.
14. Erwin PM, Olson JB, Thacker RW, (2011) Phylogenetic diversity, host-specificity and community profiling of sponge-associated bacteria in the northern Gulf of Mexico. PLoS ONE, 6, e26806.
15. Fan L, Reynolds D, Liu M, et al,. (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proceedings of the National Academy of Sciences of the United States of America, 109, E1878-E1887.
16. Fieseler L, Horn M, Wagner M, Hentschel U, (2004) Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Applied and Environment Microbiology, 70, 3724-3732.
17. Gihring TM, Green SJ, Schadt CW, (2012) Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environmental Microbiology, 14, 285-290.
18. Giles EC, Kamke J, Moitinho-Silva L, et al,. (2013) Bacterial community profiles in low microbial abundance sponges. FEMS Microbiology Ecology, 83, 232-241.
19. Gloeckner V, Hentschel U, Ereskovsky A, Schmitt S, (2013 a) Unique and species-specific microbial communities in Oscarella lobularis and other Mediterranean Oscarella species (Porifera: Homoscleromorpha). Marine Biology, 160, 781-791.
20. Gloeckner V, Lindquist N, Schmitt S, Hentschel U, (2013 b) Ectyoplasia ferox, an experimentally tractable model for vertical microbial transmission in marine sponges. Microbial Ecology, 65, 462-474.
21. Gonzalez JM, Zimmermann J, Saiz-Jimenez C, (2005) Evaluating putative chimeric sequences from PCR-amplified products. Bioinformatics, 21, 333-337.
22. Haas BJ, Gevers D, Earl AM, et al,. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494-504.
23. Hentschel U, Hopke J, Horn M, et al,. (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environment Microbiology, 68, 4431-4440.
24. Hentschel U, Fieseler L, Wehrl M, et al,. (2003) Microbial diversity of marine sponges. Progress in Molecular and Subcellular Biology, 37, 59-88.
25. Hentschel U, Usher KM, Taylor MW, (2006) Marine sponges as microbial fermenters. FEMS Microbiology Ecology, 55, 167-177.
26. Hentschel U, Piel J, Degnan SM, Taylor MW, (2012) Genomic insights into the marine sponge microbiome. Nature Reviews Microbiology, 10, 641-654.
27. Hurlbert SH, (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52, 577-586.
28. Jackson SA, Kennedy J, Morrissey JP, O'Gara F, Dobson AD, (2012) Pyrosequencing reveals diverse and distinct sponge-specific microbial communities in sponges from a single geographical location in Irish waters. Microbial Ecology, 64, 105-116.
29. Kamke J, Taylor MW, Schmitt S, (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME Journal, 4, 498-508.
30. Kuczynski J, Lauber CL, Walters WA, et al,. (2012) Experimental and analytical tools for studying the human microbiome. Nature Reviews Genetics, 13, 47-58.
31. Lanzen A, Jorgensen SL, Bengtsson MM, et al,. (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiology Ecology, 77, 577-589.
32. Lee OO, Wang Y, Yang J, et al,. (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME Journal, 5, 650-664.
33. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environment Microbiology, 71, 8228-8235.
34. Montalvo NF, Hill RT, (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Applied and Environment Microbiology, 77, 7207-7216.
35. Ngugi DK, Antunes A, Brune A, Stingl U, (2012) Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Molecular Ecology, 21, 388-405.
36. Oksanen J, Blanchet FG, Kindt R, et al,. (2012) Vegan: Community Ecology Package. Available from http://CRAN.R-project.org/package=vegan.
37. Parks DH, Beiko RG, (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics, 26, 715-721.
38. Peet RK, (1974) The measurement of species diversity. Annual Review of Ecology and Systematics, 5, 285-307.
39. Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J, (2009) Metagenomic pyrosequencing and microbial identification. Clinical Chemistry, 55, 856-866.
40. Pham VD, Konstantinidis KT, Palden T, DeLong EF, (2008) Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environmental Microbiology, 10, 2313-2330.
41. Pruesse E, Quast C, Knittel K, et al,. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research, 35, 7188-7196.
42. Rivals I, Personnaz L, Taing L, Potier MC, (2007) Enrichment or depletion of a GO category within a class of genes: which test? Bioinformatics, 23, 401-407.
43. Schloss PD, Westcott SL, Ryabin T, et al,. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environment Microbiology, 75, 7537-7541.
44. Schmitt S, Wehrl M, Lindquist N, Weisz JB, Hentschel U, (2007) Morphological and molecular analyses of microorganisms in Caribbean reef adult sponges and in corresponding reproductive material. In: Porifera Research: Biodiversity, Innovation and Sustainability (eds, Custõdio MR, Lôbo-Hajdu G, Hajdu E, &, Muricy G,), pp. 561-568. Museu Nacional, Rio de Janeiro.
45. Schmitt S, Hentschel U, Taylor M, (2012a) Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia, 687, 341-351.
46. Schmitt S, Tsai P, Bell J, et al,. (2012b) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME Journal, 6, 564-576.
47. Shannon CE, (1948) A mathematical theory of communication. Bell System Technical Journal, 27, 379-423.
48. Simister R, Taylor MW, Tsai P, et al,. (2012a) Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, Rhopaloeides odorabile. Environmental Microbiology, 14, 3232-3246.
49. Simister R, Taylor MW, Tsai P, Webster N, (2012b) Sponge-microbe associations survive high nutrients and temperatures. PLoS ONE, 7, e52220.
50. Simister RL, Deines P, Botte ES, Webster NS, Taylor MW, (2012c) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environmental Microbiology, 14, 517-524.
51. Simpson EH, (1949) Measurement of diversity. Nature, 163, 688-688.
52. Smyth GK, (2005) Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor (eds, Gentleman R, Carey V, Dudoit S, Irizarry R, &, Huber W,), pp. 397-420. Springer, New York.
53. Sogin ML, Morrison HG, Huber JA, et al,. (2006) Microbial diversity in the deep sea and the underexplored "rare biosphere". Proceedings of the National Academy of Sciences of the United States of America, 103, 12115-12120.
54. Taylor MW, Radax R, Steger D, Wagner M, (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews, 71, 295-347.
55. Taylor MW, Tsai P, Simister RL, et al,. (2013) 'Sponge-specific' bacteria are widespread (but rare) in diverse marine environments. ISME Journal, 7, 438-443.
56. Vacelet J, Donadey C, (1977) Electron microscope study of the association between some sponges and bacteria. Journal of Experimental Marine Biology and Ecology, 30, 301-314.
57. Walters WA, Caporaso JG, Lauber CL, et al,. (2011) PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics, 27, 1159-1161.
58. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environment Microbiology, 73, 5261-5267.
59. Webster NS, Taylor MW, Behnam F, et al,. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology, 12, 2070-2082.
60. Webster NS, Luter HM, Soo RM, et al,. (2012) Same, same but different: symbiotic bacterial associations in GBR sponges. Frontiers in Microbiology, 3, 444.
61. 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.
62. White JR, Patel J, Ottesen A, et al,. (2012) Pyrosequencing of bacterial symbionts within Axinella corrugata sponges: diversity and seasonal variability. PLoS ONE, 7, e38204.
63. Whitfield J, (2005) Biogeography. Is everything everywhere? Science, 310, 960-961.
64. von Wintzingerode F, Göbel UB, Stackebrandt E, (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiology Reviews, 21, 213-229.