Disturbance induced decoupling between host genetics and composition of the associated microbiome

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Wegner, Karl Mathias ^a   Volkenborn, Nils ^a,b,c   Peter, Hannes ^d   Eiler, Alexander ^e  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c IFREMER   (France)

^d UNIVERSITY OF INNSBRUCK   (Austria)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

Biological invasion; Crassostrea gigas; Microbiota; Mycoplasma; Pacific oyster; Pathogen; Population structure; Stress; Vibrio

Indexed keywords

RNA 16S;

AMPLICON; ARTICLE; CRASSOSTREA GIGAS; GENE SEQUENCE; GENETIC DISTANCE; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; GILL; HOST PARASITE INTERACTION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; MICROSATELLITE MARKER; MULTIDIMENSIONAL SCALING; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION GENETIC STRUCTURE; STRESS;

BACTERIA (MICROORGANISMS); CRASSOSTREA GIGAS; MYCOPLASMA; OSTREIDAE; SPHINGOMONAS; VIBRIO;

ANIMALS; BACTERIA; CRASSOSTREA; GASTROINTESTINAL TRACT; GILLS; MICROBIOTA; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; STRESS, PHYSIOLOGICAL;

EID: 84887078501     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-252     Document Type: Article

References (63)

1. Emerging Marine Diseases-Climate Links and Anthropogenic Factors. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, et al. Science 1999 285 5433 1505 1510 10.1126/science.285.5433.1505 10498537 (Pubitemid 29420569)
2. Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. Li Y, Qin J, Abbott C, Li X, Benkendorff K, Am J Physiol Regul Integr Comp Physiol 2007 293 6 2353 R2362 10.1152/ajpregu.00463.2007 17898119 (Pubitemid 350224029)
3. Bacterial disease in marine bivalves, a review of recent studies: Trends and evolution. Paillard C, Le Roux F, Borrego J, Aquat Living Resour 2004 17 4 477 498 10.1051/alr:2004054 (Pubitemid 40059482)
4. Herpes virus in juvenile Pacific oysters Crassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes. Friedman CS, Estes RM, Stokes NA, Burge CA, Hargove JS, Barber BJ, Elston RA, Burreson EM, Reece KS, Dis Aquat Organ 2005 63 1 33 41 15759798 (Pubitemid 40263271)
5. Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Garnier M, Labreuche Y, Garcia C, Robert A, Nicolas JL, Microb Ecol 2007 53 2 187 196 10.1007/s00248-006-9061-9 17245611
6. Summer mortality of Crassostrea gigas (Thunberg) in relation to environmental rearing conditions. Soletchnik P, Lambert C, Costil K, J Shellfish Res 2005 24 1 197 207 (Pubitemid 40697695)
7. Microarray Analysis Highlights Immune Response of Pacific Oysters as a Determinant of Resistance to Summer Mortality. Fleury E, Huvet A, Marine Biotechnol 2012 14 2 203 217 10.1007/s10126-011-9403-6
8. Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Samain JF, Degremont L, Soletchnik P, Haure J, Bedier E, Ropert M, Moal J, Huvet A, Bacca H, Van Wormhoudt A, et al. Aquaculture 2007 268 1-4 227 243 (Pubitemid 47023090)
9. Relative contribution of reproductive investment, thermal stress and Vibrio infection to summer mortality phenomena in Pacific oytsers. Wendling CC, Wegner KM, Aquaculture 2013 412-413 88 96
10. Ecological immunology. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT, Philos Trans R Soc B Biol Sci 2009 364 1513 3 14 10.1098/rstb.2008.0249
11. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. Zilber-Rosenberg I, Rosenberg E, FEMS Microbiol Rev 2008 32 5 723 735 10.1111/j.1574-6976.2008.00123.x 18549407
12. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Dubilier N, Bergin C, Lott C, Nat Rev Microbiol 2008 6 10 725 740 10.1038/nrmicro1992 18794911
13. Vibrios isolated from the cultured manila clam (Ruditapes philippinarum): numerical taxonomy and antibacterial activities. Castro D, Pujalte MJ, Lopez-Cortes L, Garay E, Borrego JJ, J Appl Microbiol 2002 93 3 438 447 10.1046/j.1365-2672.2002.01709.x 12174042 (Pubitemid 36002448)
14. Review of probiotics for use in bivalve hatcheries. Prado S, Romalde JL, Barja JL, Vet Microbiol 2010 145 3-4 187 197 20851536
15. Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi. Green TJ, Barnes AC, J Appl Microbiol 2010 109 2 613 622 20202017
16. Identification of bacterial diversity in the oyster Crassostrea gigas by fluorescent in situ hybridization and polymerase chain reaction. Hernandez-Zarate G, Olmos-Soto J, J Appl Microbiol 2006 100 4 664 672 10.1111/j.1365-2672.2005.02800.x 16553721
17. Analysis of Stomach and Gut Microbiomes of the Eastern Oyster (Crassostrea virginica) from Coastal Louisiana, USA. King GM, Judd C, Kuske CR, Smith C, PLoS ONE 2012 7 12
18. Composition and dynamics of the gill microbiota of an invasive Indo-Pacific oyster in the eastern Mediterranean Sea. Zurel D, Benayahu Y, Or A, Kovacs A, Gophna U, Environ Microbiol 2011 13 6 1467 1476 10.1111/j.1462-2920. 2011.02448.x 21635673
19. Molecular analysis of the bacterial communities in the live Pacific oyster (Crassostrea gigas) and the influence of postharvest temperature on its structure. Fernandez-Piquer J, Bowman JP, Ross T, Tamplin ML, J Appl Microbiol 2012 112 6 1134 1143 10.1111/j.1365-2672.2012.05287.x 22429335
20. Microbial diversity in the deep sea and the underexplored "rare biosphere" Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ, Proc Natl Acad Sci USA 2006 103 32 12115 12120 10.1073/pnas.0605127103 16880384 (Pubitemid 44215820)
21. Pacific oysters invade mussel beds in the European Wadden Sea. Reise K, Senckenbergiana maritima 1998 28 167 175 10.1007/BF03043147
22. High mortality of Pacific oysters in a cold winter in the North-Frisian Wadden Sea. Buttger H, Nehls G, Witte S, Helgoland Mar Res 2011 65 4 525 532 10.1007/s10152-011-0272-1
23. Invasion genetics of Pacific oyster Crassostrea gigas shaped by aquaculture stocking practices. Moehler J, Wegner KM, Reise K, Jacobsen S, J Sea Res 2011 66 3 256 262 10.1016/j.seares.2011.08.004
24. Pathology and mass mortality of Pacific oysters, Crassostrea gigas (Thunberg), in 2005 at the East Frisian coast, Germany. Watermann BT, Herlyn M, Daehne B, Bergmann S, Meemken M, Kolodzey H, J Fish Dis 2008 31 621 630 10.1111/j.1365-2761.2008.00953.x 18700939 (Pubitemid 351951912)
25. The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Linnenbrink M, Wang J, Hardouin EA, Kuenzel S, Metzler D, Baines JF, Mol Ecol 2013 22 7 1904 1916 10.1111/mec.12206 23398547
26. Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Hedgecock D, Pudovkin AI, Bull Mar Sci 2011 87 4 971 1002 10.5343/bms.2010.1051
27. Seasonal Dynamics and Modeling of a Vibrio Community in Coastal Waters of the North Sea. Oberbeckmann S, Fuchs BM, Meiners M, Wichels A, Wiltshire KH, Gerdts G, Microb Ecol 2012 63 3 543 551 10.1007/s00248-011-9990-9 22202887
28. Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: The influence of temperature and nutrients on health and survival. Malham SK, Cotter E, O'Keeffe S, Lynch S, Culloty SC, King JW, Latchford JW, Beaumont AR, Aquaculture 2009 287 1-2 128 138
29. Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D, Mol Ecol Notes 2003 3 2 228 232 10.1046/j.1471-8286.2003.00406.x (Pubitemid 36720151)
30. Linkage maps of microsatellite DNA markers for the pacific oyster Crassostrea gigas. Hubert S, Hedgecock D, Genetics 2004 168 1 351 362 10.1534/genetics.104.027342 15454548 (Pubitemid 39346600)
31. An economic method for the fluorescent labeling of PCR fragments. Schuelke M, Nat Biotechnol 2000 18 2 233 234 10.1038/72708 10657137 (Pubitemid 30091190)
32. Estimating F-Statistics for the Analysis of Population-Structure. Weir BS, Cockerham CC, Evolution 1984 38 6 1358 1370 10.2307/2408641
33. Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. Hedgecock D, Li G, Hubert S, Bucklin K, Ribes V, J Shellfish Res 2004 23 2 379 385 (Pubitemid 39283063)
34. Microsatellite null alleles and estimation of population differentiation. Chapuis MP, Estoup A, Mol Biol Evol 2007 24 3 621 631 17150975 (Pubitemid 46355787)
35. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Excoffier L, Smouse PE, Quattro JM, Genetics 1992 131 479 491 1644282
36. Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Huber J, Morrison H, Huse S, Neal P, Sogin M, Mark Welch D, Environ Microbiol 2009 11 5 1292 1302 10.1111/j.1462-2920.2008. 01857.x 19220394
37. The Use of Coded PCR Primers Enables High-Throughput Sequencing of Multiple Homolog Amplification Products by 454 Parallel Sequencing. Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, Nielsen R, Willerslev E, PLoS ONE 2007 2 2 197 10.1371/journal.pone.0000197 17299583
38. Diversity of immune genes and associated gill microbes of European plaice Pleuronectes platessa. Wegner KM, Shama LNS, Kellnreitner F, Pockberger M, Estuar Coast Shelf Sci 2012 108 87 96
39. Removing Noise From Pyrosequenced Amplicons. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ, Bmc Bioinformatics 2011 12 38 10.1186/1471-2105-12- 38 21276213
40. QIIME allows analysis of high-throughput community sequencing data. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. Nat Methods 2010 7 5 335 336 10.1038/nmeth.f.303 20383131
41. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Wang Q, Garrity GM, Tiedje JM, Cole JR, Appl Environ Microbiol 2007 73 16 5261 5267 10.1128/AEM.00062-07 17586664 (Pubitemid 47326658)
42. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P, Environ Microbiol 2010 12 1 118 123 10.1111/j.1462-2920.2009. 02051.x 19725865
43. Austin B, Austin DA, Bacterial Fish Pathogens-Disease of Farmed and Wild Fish Berlin: Springer 4 2007
44. R Development Core Team, R: A language and environment for statistical computing Vienna: R Foundation for Statistical Computing 2012
45. Abundance-occupancy relationships. Gaston KJ, Blackburn TM, Greenwood JJD, Gregory RD, Quinn RM, Lawton JH, J Appl Ecol 2000 37 39 59 10.1046/j.1365-2664.2000.00485.x
46. Using network analysis to explore co-occurrence patterns in soil microbial communities. Barberan A, Bates ST, Casamayor EO, Fierer N, ISME J 2012 6 2 343 351 10.1038/ismej.2011.119 21900968
47. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. van der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW, Carroll MP, Parkhill J, Bruce KD, ISME J 2011 5 5 780 791 10.1038/ismej.2010.175 21151003
48. Daily follow-up of bacterial communities in the human gut reveals stable composition and host-specific patterns of interaction. Durban A, Abellan JJ, Jimenez-Hernandez N, Latorre A, Moya A, FEMS Microbiol Ecol 2012 81 2 427 437 10.1111/j.1574-6941.2012.01368.x 22443608
49. Composition and Stability of the Microbial Community inside the Digestive Tract of the Aquatic Crustacean Daphnia magna. Freese HM, Schink B, Microb Ecol 2011 62 4 882 894 10.1007/s00248-011-9886-8 21667195
50. Robustness of the Bacterial Community in the Cabbage White Butterfly Larval Midgut. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J, Microb Ecol 2010 59 2 199 211 10.1007/s00248-009-9595-8 19924467
51. Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. Vanhoutte T, Huys G, De Brandt E, Swings J, FEMS Microbiol Ecol 2004 48 3 437 446 10.1016/j.femsec.2004.03.001 19712312 (Pubitemid 38648930)
52. Diversity, stability and resilience of the human gut microbiota. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R, Nature 2012 489 220 230 10.1038/nature11550 22972295
53. Viruses in the faecal microbiota of monozygotic twins and their mothers. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI, Nature 2010 466 7304 334 U381 10.1038/nature09199 20631792
54. Microbial Community Profiling to Investigate Transmission of Bacteria Between Life Stages of the Wood-Boring Beetle, Anoplophora glabripennis. Geib SM, Jimenez-Gasco MM, Carlson JE, Tien M, Jabbour R, Hoover K, Microb Ecol 2009 58 1 199 211 10.1007/s00248-009-9501-4 19277770
55. Vertical and horizontal transmission of intestinal commensal bacteria in the rat model. Inoue R, Ushida K, FEMS Microbiol Ecol 2003 46 2 213 219 10.1016/S0168-6496(03)00215-0 19719575 (Pubitemid 37338507)
56. Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Li G, Hedgecock D, Can J Fish Aquat Sci 1998 55 4 1025 1033 10.1139/f97-312 (Pubitemid 28367700)
57. Linkage disequilibrium in subdivided populations. Nei M, Li W-H, Genetics 1973 75 213 219 4762877
58. Diversity and dynamics of rare and of resident bacterial populations in coastal sands. Gobet A, Boer SI, Huse SM, van Beusekom JEE, Quince C, Sogin ML, Boetius A, Ramette A, ISME J 2012 6 3 542 553 10.1038/ismej.2011.132 21975598
59. A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet SA, Dis Aquat Organ 2001 46 139 145 11678229 (Pubitemid 32948809)
60. Bacterial 16S rRNA gene analysis revealed that bacteria related to Arcobacter spp. constitute an abundant and common component of the oyster microbiota (Tiostrea chilensis). Romero J, Garcia-Varela M, Laclette JP, Espejo RT, Microb Ecol 2002 44 4 365 371 10.1007/s00248-002-1063-7 12399898 (Pubitemid 36941367)
61. Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Gonzalez JM, Moran MA, Appl Environ Microbiol 1997 63 9361410 4237 4242 9361410 (Pubitemid 27485745)
62. Blooms of single bacterial species in a coastal lagoon of the southwestern Atlantic Ocean. Piccini C, Conde D, Alonso C, Sommaruga R, Pernthaler J, Appl Environ Microbiol 2006 72 10 6560 6568 10.1128/AEM.01089-06 17021206 (Pubitemid 44582894)
63. Bacterial composition and succession during storage of North-Atlantic cod (Gadus morhua) at superchilled temperatures. Reynisson E, Lauzon HL, Magnusson H, Jonsdottir R, Olafsdotir G, Marteinsson V, Hreggvidsson GO, BMC Microbiol 2009 9 19961579 250 19961579