Host and environmental specificity in bacterial communities associated to two highly invasive marine species (genus Asparagopsis)

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  Aires, Tânia ^a   Serrão, Ester A ^a   Engelen, Aschwin H ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Adaptation; Asparagopsis sp.; Bacterial communities; Coastal vs. off shore areas; Eco physiological functioning bacteria; Metagenomes; Polluted vs. pristine environments

Indexed keywords

QUINOLINE DERIVED ANTIINFECTIVE AGENT;

ANALYSIS OF VARIANCE; ARTICLE; BIOSYNTHESIS; CLUSTER ANALYSIS; CONTROLLED STUDY; DETOXIFICATION; DNA EXTRACTION; ENVIRONMENTAL PROTECTION; MARINE SPECIES; METAGENOMICS; MICROBIAL COMMUNITY; MORPHOGENESIS; NONHUMAN; OXIDATIVE STRESS; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS;

EID: 84966280536     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00559     Document Type: Article

References (68)

1. Abbott, I. A. (1999). Marine Red Algae of the Hawaiian Islands. Honolulu, HI: Bishop Museum Press
2. Abraham, W. R., Strömpl, C., Meyer, H., Lindholst, S., Moore, E. R., Christ, R., et al. (1999). Phylogeny and polyphasic taxonomy of Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundimonas and Caulobacter. Int. J. Syst. Bacteriol. 49(Pt 3), 1053-1073. doi: 10.1099/00207713-49-3-1053
3. Ainsworth, T., Krause, L., Bridge, T., Torda, G., Raina, J.-B., Zakrzewski, M., et al. (2015). The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261-2274. doi: 10.1038/ismej.2015.39
4. Aires, T., Moalic, Y., Serrao, E. A., and Arnaud-Haond, S. (2015). Hologenome theory supported by co-occurrence networks of species-specific bacterial communities in siphonous algae (Caulerpa). FEMS Microbiol. Ecol. 91:fiv067. doi: 10.1093/femsec/fiv067
5. Aires, T., Serrão, E. A., Kendrick, G., Duarte, C. M., and Arnaud-Haond, S. (2013). Invasion is a community affair: Clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa, track the invasion source. PLoS ONE 8:e68429. doi: 10.1371/journal.pone.0068429
6. Alain, K., Tindall, B. J., Intertaglia, L., Catala, P., and Lebaron, P. (2008). Hellea balneolensis gen. nov., sp. nov., a prosthecate alphaproteobacterium from the Mediterranean Sea. Int. J. Syst. Evol. Microbiol. 58, 2511-2519. doi: 10.1099/ijs.0.65424-0
7. Alonso-Gutiérrez, J., Figueras, A., Albaigés, J., Jiménez, N., Viñas, M., Solanas, A. M., et al. (2009). Bacterial communities from shoreline environments (Costa da Morte, northwestern Spain) affected by the Prestige oil spill. Appl. Environ. Microbiol. 75, 3407-3418. doi: 10.1128/AEM.01776-08
8. Anast, N., and Smit, J. (1988). Isolation and characterization of marine caulobacters and assessment of their potential for genetic experimentation. Appl. Environ. Microbiol. 54, 809-817
9. Andreakis, N., Kooistra, W. H. C. F., and Procaccini, G. (2009). High genetic diversity and connectivity in the polyploid invasive seaweed Asparagopsis taxiformis (Bonnemaisoniales) in the Mediterranean, explored with microsatellite alleles and multilocus genotypes. Mol. Ecol. 18, 212-226. doi: 10.1111/j.1365-294X.2008.04022.x
10. Andreakis, N., Procaccini, G., and Kooistra, W. H. (2004). Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Rhodophyta): genetic and morphological identification of Mediterranean populations. Eur. J. Phycol. 39, 273-283. doi: 10.1080/0967026042000236436
11. Andreakis, N., Procaccini, G., Maggs, C., and Kooistra, W. H. C. F. (2007). Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol. Ecol. 16, 2285-2299. doi: 10.1111/j.1365-294X.2007.03306.x
12. Anonymous (2008). Plano de Ordenamento do Parque Natural Do Sudoeste Alentejano e Costa Vicentina-Fase 2-Diagnóstico. Volume I/II. Lisbon: ICN-Instituto de Conservação da Natureza
13. Barott, K. L., Rodriguez-Brito, B., Janouškovec, J., Marhaver, K. L., Smith, J. E., Keeling, P., et al. (2011). Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ. Microbiol. 13, 1192-1204. doi: 10.1111/j.1462-2920.2010.02419.x
14. Biddanda, B., Ogdahl, M., and Cotner, J. (2001). Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol. Oceanogr. 46, 730-739. doi: 10.4319/lo.2001.46.3.0730
15. Bray, J. R., and Curtis, J. T. (1957). An Ordination of the upland forest community of southern Wisconsin.pdf. Ecol. Monogr. 27, 325-349. doi: 10.2307/1942268
16. Bridle, J. R., and Vines, T. H. (2007). Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol. Evol. 22, 140-147. doi: 10.1016/j.tree.2006.11.002
17. Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S., and Thomas, T. (2011). Bacterial community assembly based on functional genes rather than species. Proc. Natl. Acad. Sci. U.S.A. 108, 14288-14293. doi: 10.1073/pnas.1101591108
18. Campbell, A. H., Marzinelli, E. M., Gelber, J., and Steinberg, P. D. (2015). Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front. Microbiol. 6:230. doi: 10.3389/fmicb.2015.00230
19. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). Correspondence QIIME allows analysis of high-throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat. Publ. Gr. 7, 335-336. doi: 10.1038/nmeth.f.303
20. Chao, A. (1984). Nonparametric estimation of the number of Classes in a population. Scand. J. Stat. 11, 265-270
21. Chisholm, J. R. M., Dauga, C., Ageron, E., Grimont, P. A. D., and Jaubert, J. M. (1996). "Roots" in mixotrophic algae. Nature 381, 382-382. doi: 10.1038/381382a0
22. Clarke, K. R., and Warwick, R. M. (1994). Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth: Plymouth Marine Laboratory, Natural Environment Research Council
23. Crump, B. C., and Koch, E. W. (2008). Attached bacterial populations shared by four species of aquatic angiosperms. Appl. Environ. Microbiol. 74, 5948-5957. doi: 10.1128/AEM.00952-08
24. Dijoux, L., Viard, F., and Payri, C. (2014). The more we search, the more we find: discovery of a new lineage and a new species complex in the genus Asparagopsis. PLoS ONE 13:e103826. doi: 10.1371/journal.pone.0103826
25. Dittami, S. M., Duboscq-Bidot, L., Perennou, M., Gobet, A., Corre, E., Boyen, C., et al. (2016). Host-microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME J. 10, 51-63. doi: 10.1038/ismej.2015.104
26. Dittami, S. M., Eveillard, D., and Tonon, T. (2014). A metabolic approach to study algal-bacterial interactions in changing environments. Mol. Ecol. 23, 1656-1660. doi: 10.1111/mec.12670
27. Dlugosch, K. M., and Parker, I. M. (2008). Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431-449. doi: 10.1111/j.1365-294X.2007.03538.x
28. Dring, M. J. (2006). Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv. Bot. Res. 43, 176-207. doi: 10.1016/S0065-2296(05)43004-9
29. European Environment Agency-EEA (2007). Halting the Loss of Biodiversity by 2010: Proposal for a First Set of Indicators to Monitor Progress in Europe. Technical Report 11/2007, European Environment Agency
30. Egan, S., Thomas, T., Holmström, C., and Kjelleberg, S. (2000). Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environ. Microbiol. 2, 343-347. doi: 10.1046/j.1462-2920.2000.00107.x
31. Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., et al. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494-504. doi: 10.1101/gr.112730.110
32. Hanshew, A. S., Mason, C. J., Raffa, K. F., and Currie, C. R. (2013). Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J. Microbiol. Methods 95, 149-155. doi: 10.1016/j.mimet.2013.08.007
33. Hester, E. R., Barott, K. L., Nulton, J., Vermeij, M. J., and Rohwer, F. L. (2016). Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. 10, 1157-1169. doi: 10.1038/ismej.2015.190
34. Hollants, J., Leliaert, F., Verbruggen, H., Willems, A., and De Clerck, O. (2013). Permanent residents or temporary lodgers: characterizing intracellular bacterial communities in the siphonous green alga Bryopsis. Proc. Biol. Sci. 280, 20122659. doi: 10.1098/rspb.2012.2659
35. Kelly, L. W., Williams, G. J., Barott, K. L., Carlson, C. A., Dinsdale, E. A., Edwards, R. A., et al. (2014). Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc. Natl. Acad. Sci. U.S.A. 111, 10227-10232. doi: 10.1073/pnas.1403319111
36. Khodjaniyazov, K. U. (2012). Degradation and detoxification of persistent organic pollutants in soils by plant alkaloid anabasine. J. Environ. Prot. (Irvine,. Calif). 3, 97-106. doi: 10.4236/jep.2012.31012
37. Lachnit, T., Meske, D., Wahl, M., Harder, T., and Schmitz, R. (2011). Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ. Microbiol. 13, 655-665. doi: 10.1111/j.1462-2920.2010.02371.x
38. Lane, D. J. (1991). "16S/23S rRNA sequencing, " in Nucleic Acid Techniques in Bacterial Systematics, eds E. Stackebrandt and M. Goodfellow (Chichester: John Wiley and Sons), 115-175
39. Lee, O. O., Chui, P. Y., Wong, Y. H., Pawlik, J. R., and Qian, P.-Y. (2009). Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl. Environ. Microbiol. 75, 6147-6156. doi: 10.1128/AEM.00023-09
40. Mandrioli, M., and Manicardi, G. C. (2013). Evolving aphids: One genome-one organism insects or holobionts? Invertebr. Surv. J. 10, 1-6
41. Marcial Gomes, N. C., Borges, L. R., Paranhos, R., Pinto, F. N., Mendonça-Hagler, L. C. S., and Smalla, K. (2008). Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol. Ecol. 66, 96-109. doi: 10.1111/j.1574-6941.2008.00519.x
42. Marzinelli, E. M., Campbell, A. H., Zozaya Valdes, E., Vergés, A., Nielsen, S., Wernberg, T., et al. (2015). Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environ. Microbiol. 17, 4078-4088. doi: 10.1111/1462-2920.12972
43. Massa, S. I., Paulino, C. M., Serrão, E. A., Duarte, C. M., and Arnaud-Haond, S. (2013). Entangled effects of allelic and clonal (genotypic) richness in the resistance and resilience of experimental populations of the seagrass Zostera noltii to diatom invasion. BMC Ecol. 13:39. doi: 10.1186/1472-6785-13-39
44. McKew, B. A., Coulon, F., Osborn, A. M., Timmis, K. N., and McGenity, T. J. (2007). Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ. Microbiol. 9, 165-176. doi: 10.1111/j.1462-2920.2006.01125.x
45. Mellado, M., Contreras, R. A., González, A., Dennett, G., and Moenne, A. (2012). Copper-induced synthesis of ascorbate, glutathione and phytochelatins in the marine alga Ulva compressa (Chlorophyta). Plant Physiol. Biochem. 51, 102-108. doi: 10.1016/j.plaphy.2011.10.007
46. Meyer, F., Paarmann, D., D'souza, M., Olson, R., Glass, E. M., Kubal, M., et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform. 9, 386. doi: 10.1186/1471-2105-9-386
47. Morrow, K. M., Ritson-Williams, R., Ross, C., Liles, M. R., and Paul, V. J. (2012). Macroalgal extracts induce bacterial assemblage shifts and sublethal tissue stress in Caribbean corals. PLoS ONE 7:e44859. doi: 10.1371/journal.pone.0044859
48. Nakanishi, K., and Nishijima, M. (1996). Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J. Phycol. 32, 479-482
49. Neave, M. J., Streten-Joyce, C., Glasby, C. J., McGuinness, K. A., Parry, D. L., and Gibb, K. S. (2012). The bacterial community associated with the marine Polychaete ophelina sp.1 (Annelida: Opheliidae) is altered by copper and zinc contamination in sediments. Microb. Ecol. 63, 639-650. doi: 10.1007/s00248-011-9966-9
50. O'Hara, A. M., and Shanahan, F. (2006). The gut flora as a forgotten organ. EMBO Rep. 7, 688-693. doi: 10.1038/sj.embor.7400731
51. Oliveira, V., Gomes, N. C. M., Cleary, D. F. R., Almeida, A., Silva, A. M. S., Simões, M. M. Q., et al. (2014). Halophyte plant colonization as a driver of the composition of bacterial communities in salt marshes chronically exposed to oil hydrocarbons. FEMS Microbiol. Ecol. 90, 647-662. doi: 10.1111/1574-6941.12425
52. Oliveros, J. C. (2007). VENNY. An Interactive Tool for Comparing Lists with Venn Diagrams. Available online at: http://bioinfogp.cnb.csic.es/tools/venny/index.html
53. Orole, O., and Adejumo, T. (2011). Bacterial and fungal endophytes associated with grains and roots of maize. J. Ecol. Nat. Env. 3, 298-303
54. Pauls, S. U., Nowak, C., Bálint, M., and Pfenninger, M. (2013). The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22, 925-946. doi: 10.1111/mec.12152
55. Pinto, E., Sigaud-Kutner, T. C. S., Leitao, M. A. S., and Okamoto, O. K. (2003). Review heavy metal-Induced oxidative stress in algae. J. Phycol. 39, 1008-1018. doi: 10.1111/j.0022-3646.2003.02-193.x
56. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596. doi: 10.1093/nar/gks1219
57. Ratkevicius, N., Correa, J. A., and Moenne, A. (2003). Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ. 26, 1599-1608. doi: 10.1046/j.1365-3040.2003.01073.x
58. Rijstenbil, J. W., Coelho, S. M., and Eijsackers, M. (2000). A method for the assessment of light-induced oxidative stress in embryos of fucoid algae via confocal laserscan microscopy. Mar. Biol. 137, 763-774. doi: 10.1007/s002270000443
59. Rosenberg, E., Koren, O., Reshef, L., Efrony, R., and Zilber-Rosenberg, I. (2007). The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355-362. doi: 10.1038/nrmicro1635
60. Rosenberg, E., Sharon, G., Atad, I., and Zilber-Rosenberg, I. (2010). The evolution of animals and plants via symbiosis with microorganisms. Environ. Microbiol. Rep. 2, 500-506. doi: 10.1111/j.1758-2229.2010.00177.x
61. Sherwood, A. R. (2008). Phylogeography of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) in the Hawaiian Islands: two Mtdna markers support three separate introductions. Phycologia 47, 79-88. doi: 10.2216/07-39.1
62. Streftaris, N., and Zenetos, A. (2006). Alien marine species in the Mediterranean-the 100 "worst invasives" and their impact. Mediterr. Mar. Sci. 7, 87-118. doi: 10.12681/mms.180
63. Thompson, J. R., Rivera, H. E., Closek, C. J., and Medina, M. (2015). Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front. Cell. Infect. Microbiol. 4:176. doi: 10.3389/fcimb.2014.00176
64. Tonon, T., Eveillard, D., Prigent, S., Bourdon, J., Potin, P., Boyen, C., et al. (2011). Toward systems biology in brown algae to explore acclimation and adaptation to the shore environment. OMICS 15, 883-892. doi: 10.1089/omi.2011.0089
65. Vincent, P., Pignet, P., Talmont, F., Bozzi, L., Fournet, B., Guezennec, J., et al. (1994). Production and characterization of an exopolysaccharide excreted by a deep-sea hydrothermal vent bacterium isolated from the polychaete annelid Alvinella pompejana. Appl. Environ. Microbiol. 60, 4134-4141
66. War, A. R., Paulraj, M. G., Ahmad, T., Buhroo, A. A., Hussain, B., Ignacimuthu, S., et al. (2012). Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 7, 1306-1320. doi: 10.4161/psb.21663
67. Zeng, Y., Ma, Y., Wei, C., Jiao, N., Tang, K., Wu, Z., et al. (2010). Bacterial diversity in various coastal mariculture ponds in Southeast China and in diseased eels as revealed by culture and culture-independent molecular techniques. Aquac. Res. 41, e172-e186. doi: 10.1111/j.1365-2109.2010.02499.x
68. Zilber-Rosenberg, I., and Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723-735. doi: 10.1111/j.1574-6976.2008.00123.x