Host rules: Spatial stability of bacterial communities associated with marine sponges (ircinia spp.) in the western mediterranean sea

FEMS Microbiology Ecology

Volumn 86, Issue 2, 2013, Pages 268-276

  Pita, Lucía ^a   Turon, Xavier ^b   López Legentil, Susanna ^a,c   Erwin, Patrick M ^a,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^c UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Biogeography; Distance decay; Host specificity; Isolation by distance; Porifera; Spatial variation; Symbiosis

Indexed keywords

RNA 16S;

BACTERIUM; COEXISTENCE; COMMUNITY STRUCTURE; DISPERSAL; HOST SPECIFICITY; ISOLATED POPULATION; MICROBIAL COMMUNITY; SPATIAL VARIATION; SPONGE; SYMBIOSIS;

ANIMAL; ARTICLE; BACTERIUM; BIOGEOGRAPHY; CLASSIFICATION; DISTANCE-DECAY; GENETICS; HOST RANGE; ISOLATION AND PURIFICATION; ISOLATION-BY-DISTANCE; MEDITERRANEAN SEA; MICROBIOLOGY; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SPATIAL VARIATION; SPONGE (PORIFERA); SYMBIOSIS;

BIOGEOGRAPHY; DISTANCE-DECAY; HOST SPECIFICITY; ISOLATION-BY-DISTANCE; PORIFERA; SPATIAL VARIATION; SYMBIOSIS;

ANIMALS; BACTERIA; MEDITERRANEAN SEA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PORIFERA; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

MEDITERRANEAN SEA; MEDITERRANEAN SEA (WEST);

BACTERIA (MICROORGANISMS); IRCINIA; IRCINIA VARIABILIS; PORIFERA;

EID: 84885954466     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12159     Document Type: Article

References (54)

1. Abdo Z, Schüette UME, Bent SJ, Williams CJ, Forney LJ & Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8: 929-938.
2. Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. Anderson M (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
4. Anderson SA, Northcote PT & Page MJ (2010) Spatial and temporal variability of the bacterial community in different chemotypes of the New Zealand marine sponge Mycale hentscheli. FEMS Microbiol Ecol 72: 328-342.
5. Benjamini Y & Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188.
6. Blanquer A & Uriz MJ (2010) Population genetics at three spatial scales of a rare sponge living in fragmented habitats. BMC Evol Biol 10: 13.
7. Clarke K (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
8. Clarke K & Gorley R (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, MA.
9. Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H & Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10: 171.
10. Dray S & Dufour A (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22: 1-20.
11. Duran S, Pascual M, Estoup A & Turon X (2004) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Mol Ecol 13: 511-522.
12. Ereskovsky AV & Tokina DB (2004) Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr Reprod Dev 45: 137-150.
13. Ereskovsky AV, Gonobobleva E & Vishnyakov A (2004) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146: 869-875.
14. Erwin PM & Thacker RW (2008) Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts. Mol Ecol 17: 2937-2947.
15. Erwin PM, López-Legentil S, González-Pech R & Turon X (2012a) A specific mix of generalists: bacterial symbionts in Mediterranean Ircinia spp. FEMS Microbiol Ecol 79: 619-637.
16. Erwin PM, Pita L, López-Legentil S & Turon X (2012b) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol 78: 7358-7368.
17. Fierer N (2008) Microbial biogeography: patterns in microbial diversity across space and time. Accessing Uncultivated Microorganisms: From the Environment to Organisms and Genomes (Zengler K, ed), pp. 95-115. ASM Press, Washington, DC.
18. Flo E, Garcés E, Manzanera M & Camp J (2011) Coastal inshore waters in the NW Mediterranean: physicochemical and biological characterization and management implications. Estuar Coast Shelf Sci 93: 279-289.
19. Galand PE, Casamayor EO, Kirchman DL & Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. P Natl Acad Sci USA 106: 22427-22432.
20. Hanson CA, Fuhrman JA, Horner-Devine MC & Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10: 497-506.
21. Hardoim CCP, Esteves AIS, Pires FR, Gonçalves JMS, Cox CJ, Xavier JR & Costa R (2012) Phylogenetically and spatially close marine sponges harbour divergent bacterial communities. PLoS ONE 7: e53029.
22. Hentschel U, Horn M, Friedrich AB, Wagner M & Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
23. Hentschel U, Piel J, Degnan SM & Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10: 641-654.
24. Kent AD, Smith DJ, Benson BJ & Triplett EW (2003) Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl Environ Microbiol 69: 6768-6776.
25. Lee OO, Wong YH & Qian P-Y (2009a) Inter- and intraspecific variations of bacterial communities associated with marine sponges from San Juan Island, Washington. Appl Environ Microbiol 75: 3513-3521.
26. Lee OO, Chui PY, Wong YH, Pawlik JR & Qian P-Y (2009b) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microbiol 75: 6147-6156.
27. Mariani S, Uriz MJ & Turon X (2005) The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms. J Plankton Res 27: 249-262.
28. Martínez-Murcia A, Acinas S & Rodríguez-Valera F (1995) Evaluation of prokaryotic diversity by restrictase digestion of 16S rDNA directly amplified from hypersaline environments. FEMS Microbiol Ecol 17: 247-255.
29. Martiny JBH, Bohannan BJM, Brown JH et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4: 102-112.
30. McArdle BH & Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290-297.
31. Millot C (1999) Circulation in the Western Mediterranean Sea. J Mar Syst 20: 423-442.
32. 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.
33. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14: 257-263.
34. Pedrós-Alió C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4: 449-466.
35. Pita L, López-Legentil S & Erwin PM (2013) Biogeography and host fidelity of bacterial communities in Ircinia spp from the Bahamas. Microb Ecol, in press DOI: 10.007/s00248-013-0215-2
36. Schauer M, Massana R & Pedrós-Alió C (2000) Spatial differences in bacterioplankton composition along the Catalan coast (NW Mediterranean) assessed by molecular fingerprinting. FEMS Microbiol Ecol 33: 51-59.
37. Schmitt S, Weisz JB, Lindquist N & Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73: 2067-2078.
38. 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.
39. Schmitt S, Tsai P, Bell J et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
40. Schöttner S, Hoffmann F, Cárdenas P, Rapp HT, Boetius A & Ramette A (2013) Relationships between host phylogeny, host type and bacterial community diversity in cold-water coral reef sponges. PLoS ONE 8: e55505.
41. Taylor MW, Schupp PJ, De Nys R, Kjelleberg S & Steinberg PD (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ Microbiol 7: 419-433.
42. Taylor MW, Radax R, Steger D & Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
43. Taylor MW, Tsai P, Simister RL, Deines P, Botte E, Ericson G, Schmitt S & Webster NS (2013) 'Sponge-specific' bacteria are widespread (but rare) in diverse marine environments. ISME J 7: 438-443.
44. The R Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
45. Thiel V, Leininger S, Schmaljohann R, Brümmer F & Imhoff JF (2007) Sponge-specific bacterial associations of the Mediterranean sponge Chondrilla nucula (Demospongiae, Tetractinomorpha). Microb Ecol 54: 101-111.
46. Turner S, Pryer KM, Miao VP & Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46: 327-338.
47. Turon X, Garriga A & Erwin PM (2013) Lights and shadows: growth patterns in three sympatric and congeneric sponges (Ircinia spp) with contrasting abundances of photosymbionts. Mar Biol, in press DOI: 10.1007/s00227-013-2267-8
48. Uriz MJ, Turon X & Mariani S (2008) Ultrastructure and dispersal potential of sponge larvae: tufted versus evenly ciliated parenchymellae. Mar Ecol 29: 280-297.
49. Usher KM, Kuo J, Fromont J & Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461: 15-23.
50. Webster NS, Negri AP, Munro MMHG & Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6: 288-300.
51. Webster NS, Taylor MW, Behnam F, Lücker 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.
52. Wichels A, Würtz S, Döpke H, Schütt C & Gerdts G (2006) Bacterial diversity in the breadcrumb sponge Halichondria panicea (Pallas). FEMS Microbiol Ecol 56: 102-118.
53. Yang J, Sun J, Lee O, Wong Y & Qian P (2011) Phylogenetic diversity and community structure of sponge-associated bacteria from mangroves of the Caribbean Sea. Aquat Microb Ecol 62: 231-240.
54. Zhang R, Thiyagarajan V & Qian P-Y (2008) Evaluation of terminal-restriction fragment length polymorphism analysis in contrasting marine environments. FEMS Microbiol Ecol 65: 169-178.