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

BMC Microbiology

Alexander Eiler⁴  Hannes Peter¹  Nils Volkenborn³  Karl Mathias Wegner² 

[1] Laboratory of Aquatic Photobiology and Plankton Ecology, Institute of Ecology, University of Innsbruck, Technikerstrasse 25, Innsbruck 6020, Austria;Helmholtz Centre for Polar and Marine Research, Alfred Wegener Institute, Coastal Ecology, Wadden Sea Station Sylt, Hafenstrasse 43, 25992, List/Sylt, Germany;Benthic Ecology Laboratory, IFREMER, DYNECO, BP70, Plouzane 29280, France;Department of Ecology and Genetcis, Uppsala University, Limnology, Norbyvägen 18D, Uppsala 75236, Sweden

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

Others  :  1142765
DOI  :  10.1186/1471-2180-13-252

 received in 2013-07-04, accepted in 2013-11-01,  发布年份 2013

【 摘 要 】

Background

Studies of oyster microbiomes have revealed that a limited number of microbes, including pathogens, can dominate microbial communities in host tissues such as gills and gut. Much of the bacterial diversity however remains underexplored and unexplained, although environmental conditions and host genetics have been implicated. We used 454 next generation 16S rRNA amplicon sequencing of individually tagged PCR reactions to explore the diversity of bacterial communities in gill tissue of the invasive Pacific oyster Crassostrea gigas stemming from genetically differentiated beds under ambient outdoor conditions and after a multifaceted disturbance treatment imposing stress on the host.

Results

While the gill associated microbial communities in oysters were dominated by few abundant taxa (i.e. Sphingomonas, Mycoplasma) the distribution of rare bacterial groups correlated to relatedness between the hosts under ambient conditions. Exposing the host to disturbance broke apart this relationship by removing rare phylotypes thereby reducing overall microbial diversity. Shifts in the microbiome composition in response to stress did not result in a net increase in genera known to contain potentially pathogenic strains.

Conclusion

The decrease in microbial diversity and the disassociation between population genetic structure of the hosts and their associated microbiome suggest that disturbance (i.e. stress) may play a significant role for the assembly of the natural microbiome. Such community shifts may in turn also feed back on the course of disease and the occurrence of mass mortality events in oyster populations.

【 授权许可】

   
2013 Wegner et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, et al.: Emerging Marine Diseases–Climate Links and Anthropogenic Factors. Science 1999, 285(5433):1505-1510.
• [2]Li Y, Qin J, Abbott C, Li X, Benkendorff K: Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. Am J Physiol Regul Integr Comp Physiol 2007, 293(6):R2353-R2362.
• [3]Paillard C, Le Roux F, Borrego J: Bacterial disease in marine bivalves, a review of recent studies: Trends and evolution. Aquat Living Resour 2004, 17(4):477-498.
• [4]Friedman CS, Estes RM, Stokes NA, Burge CA, Hargove JS, Barber BJ, Elston RA, Burreson EM, Reece KS: Herpes virus in juvenile Pacific oysters Crassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes. Dis Aquat Organ 2005, 63(1):33-41.
• [5]Garnier M, Labreuche Y, Garcia C, Robert A, Nicolas JL: Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 2007, 53(2):187-196.
• [6]Soletchnik P, Lambert C, Costil K: Summer mortality of Crassostrea gigas (Thunberg) in relation to environmental rearing conditions. J Shellfish Res 2005, 24(1):197-207.
• [7]Fleury E, Huvet A: Microarray Analysis Highlights Immune Response of Pacific Oysters as a Determinant of Resistance to Summer Mortality. Marine Biotechnol 2012, 14(2):203-217.
• [8]Samain JF, Degremont L, Soletchnik P, Haure J, Bedier E, Ropert M, Moal J, Huvet A, Bacca H, Van Wormhoudt A, et al.: Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 2007, 268(1–4):227-243.
• [9]Wendling CC, Wegner KM: Relative contribution of reproductive investment, thermal stress and Vibrio infection to summer mortality phenomena in Pacific oytsers. Aquaculture 2013, 412-413:88-96.
• [10]Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT: Ecological immunology. Philos Trans R Soc B Biol Sci 2009, 364(1513):3-14.
• [11]Zilber-Rosenberg I, Rosenberg E: Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 2008, 32(5):723-735.
• [12]Dubilier N, Bergin C, Lott C: Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 2008, 6(10):725-740.
• [13]Castro D, Pujalte MJ, Lopez-Cortes L, Garay E, Borrego JJ: Vibrios isolated from the cultured manila clam (Ruditapes philippinarum): numerical taxonomy and antibacterial activities. J Appl Microbiol 2002, 93(3):438-447.
• [14]Prado S, Romalde JL, Barja JL: Review of probiotics for use in bivalve hatcheries. Vet Microbiol 2010, 145(3–4):187-197.
• [15]Green TJ, Barnes AC: Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi. J Appl Microbiol 2010, 109(2):613-622.
• [16]Hernandez-Zarate G, Olmos-Soto J: Identification of bacterial diversity in the oyster Crassostrea gigas by fluorescent in situ hybridization and polymerase chain reaction. J Appl Microbiol 2006, 100(4):664-672.
• [17]King GM, Judd C, Kuske CR, Smith C: Analysis of Stomach and Gut Microbiomes of the Eastern Oyster (Crassostrea virginica) from Coastal Louisiana, USA. PLoS ONE 2012, 7:12.
• [18]Zurel D, Benayahu Y, Or A, Kovacs A, Gophna U: Composition and dynamics of the gill microbiota of an invasive Indo-Pacific oyster in the eastern Mediterranean Sea. Environ Microbiol 2011, 13(6):1467-1476.
• [19]Fernandez-Piquer J, Bowman JP, Ross T, Tamplin ML: Molecular analysis of the bacterial communities in the live Pacific oyster (Crassostrea gigas) and the influence of postharvest temperature on its structure. J Appl Microbiol 2012, 112(6):1134-1143.
• [20]Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ: Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 2006, 103(32):12115-12120.
• [21]Reise K: Pacific oysters invade mussel beds in the European Wadden Sea. Senckenbergiana maritima 1998, 28:167-175.
• [22]Buttger H, Nehls G, Witte S: High mortality of Pacific oysters in a cold winter in the North-Frisian Wadden Sea. Helgoland Mar Res 2011, 65(4):525-532.
• [23]Moehler J, Wegner KM, Reise K, Jacobsen S: Invasion genetics of Pacific oyster Crassostrea gigas shaped by aquaculture stocking practices. J Sea Res 2011, 66(3):256-262.
• [24]Watermann BT, Herlyn M, Daehne B, Bergmann S, Meemken M, Kolodzey H: Pathology and mass mortality of Pacific oysters, Crassostrea gigas (Thunberg), in 2005 at the East Frisian coast, Germany. J Fish Dis 2008, 31:621-630.
• [25]Linnenbrink M, Wang J, Hardouin EA, Kuenzel S, Metzler D, Baines JF: The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol 2013, 22(7):1904-1916.
• [26]Hedgecock D, Pudovkin AI: Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 2011, 87(4):971-1002.
• [27]Oberbeckmann S, Fuchs BM, Meiners M, Wichels A, Wiltshire KH, Gerdts G: Seasonal Dynamics and Modeling of a Vibrio Community in Coastal Waters of the North Sea. Microb Ecol 2012, 63(3):543-551.
• [28]Malham SK, Cotter E, O’Keeffe S, Lynch S, Culloty SC, King JW, Latchford JW, Beaumont AR: Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: The influence of temperature and nutrients on health and survival. Aquaculture 2009, 287(1–2):128-138.
• [29]Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D: Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Mol Ecol Notes 2003, 3(2):228-232.
• [30]Hubert S, Hedgecock D: Linkage maps of microsatellite DNA markers for the pacific oyster Crassostrea gigas. Genetics 2004, 168(1):351-362.
• [31]Schuelke M: An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 2000, 18(2):233-234.
• [32]Weir BS, Cockerham CC: Estimating F-Statistics for the Analysis of Population- Structure. Evolution 1984, 38(6):1358-1370.
• [33]Hedgecock D, Li G, Hubert S, Bucklin K, Ribes V: Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. J Shellfish Res 2004, 23(2):379-385.
• [34]Chapuis MP, Estoup A: Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 2007, 24(3):621-631.
• [35]Excoffier L, Smouse PE, Quattro JM: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131:479-491.
• [36]Huber J, Morrison H, Huse S, Neal P, Sogin M, Mark Welch D: Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 2009, 11(5):1292-1302.
• [37]Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, Nielsen R, Willerslev E: The Use of Coded PCR Primers Enables High-Throughput Sequencing of Multiple Homolog Amplification Products by 454 Parallel Sequencing. PLoS ONE 2007, 2(2):e197.
• [38]Wegner KM, Shama LNS, Kellnreitner F, Pockberger M: Diversity of immune genes and associated gill microbes of European plaice Pleuronectes platessa. Estuar Coast Shelf Sci 2012, 108:87-96.
• [39]Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ: Removing Noise From Pyrosequenced Amplicons. Bmc Bioinformatics 2011, 12:38. BioMed Central Full Text
• [40]Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al.: QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7(5):335-336.
• [41]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267.
• [42]Kunin V, Engelbrektson A, Ochman H, Hugenholtz P: Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 2010, 12(1):118-123.
• [43]Austin B, Austin DA: Bacterial Fish Pathogens - Disease of Farmed and Wild Fish. 4th edition. Berlin: Springer; 2007.
• [44]R Development Core Team: R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2012.
• [45]Gaston KJ, Blackburn TM, Greenwood JJD, Gregory RD, Quinn RM, Lawton JH: Abundance-occupancy relationships. J Appl Ecol 2000, 37:39-59.
• [46]Barberan A, Bates ST, Casamayor EO, Fierer N: Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 2012, 6(2):343-351.
• [47]van der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW, Carroll MP, Parkhill J, Bruce KD: Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J 2011, 5(5):780-791.
• [48]Durban A, Abellan JJ, Jimenez-Hernandez N, Latorre A, Moya A: Daily follow-up of bacterial communities in the human gut reveals stable composition and host-specific patterns of interaction. FEMS Microbiol Ecol 2012, 81(2):427-437.
• [49]Freese HM, Schink B: Composition and Stability of the Microbial Community inside the Digestive Tract of the Aquatic Crustacean Daphnia magna. Microb Ecol 2011, 62(4):882-894.
• [50]Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J: Robustness of the Bacterial Community in the Cabbage White Butterfly Larval Midgut. Microb Ecol 2010, 59(2):199-211.
• [51]Vanhoutte T, Huys G, De Brandt E, Swings J: Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol Ecol 2004, 48(3):437-446.
• [52]Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R: Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489:220-230.
• [53]Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI: Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010, 466(7304):334-U381.
• [54]Geib SM, Jimenez-Gasco MM, Carlson JE, Tien M, Jabbour R, Hoover K: Microbial Community Profiling to Investigate Transmission of Bacteria Between Life Stages of the Wood-Boring Beetle, Anoplophora glabripennis. Microb Ecol 2009, 58(1):199-211.
• [55]Inoue R, Ushida K: Vertical and horizontal transmission of intestinal commensal bacteria in the rat model. FEMS Microbiol Ecol 2003, 46(2):213-219.
• [56]Li G, Hedgecock D: Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Can J Fish Aquat Sci 1998, 55(4):1025-1033.
• [57]Nei M, Li W-H: Linkage disequilibrium in subdivided populations. Genetics 1973, 75:213-219.
• [58]Gobet A, Boer SI, Huse SM, van Beusekom JEE, Quince C, Sogin ML, Boetius A, Ramette A: Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 2012, 6(3):542-553.
• [59]Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet SA: A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Organ 2001, 46:139-145.
• [60]Romero J, Garcia-Varela M, Laclette JP, Espejo RT: Bacterial 16S rRNA gene analysis revealed that bacteria related to Arcobacter spp. constitute an abundant and common component of the oyster microbiota (Tiostrea chilensis). Microb Ecol 2002, 44(4):365-371.
• [61]Gonzalez JM, Moran MA: Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 1997, 63(9361410):4237-4242.
• [62]Piccini C, Conde D, Alonso C, Sommaruga R, Pernthaler J: Blooms of single bacterial species in a coastal lagoon of the southwestern Atlantic Ocean. Appl Environ Microbiol 2006, 72(10):6560-6568.
• [63]Reynisson E, Lauzon HL, Magnusson H, Jonsdottir R, Olafsdotir G, Marteinsson V, Hreggvidsson GO: Bacterial composition and succession during storage of North-Atlantic cod (Gadus morhua) at superchilled temperatures. BMC Microbiol 2009, 9(19961579):250.