Hologenome theory supported by cooccurrence networks of Species-specific bacterial communities in siphonous algae (Caulerpa)

FEMS Microbiology Ecology

Volumn 91, Issue 7, 2015, Pages

  Aires, Tania ^a   Moalic, Yann ^b,c   Serrao, Ester A ^a   Arnaud Haond, Sophie ^a,d  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b Institut Paul Emile Victor Technopole Brest Iroise   (France)

^c INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

^d UNIVERSITÉ MONTPELLIER 2   (France)

Author keywords

Bacterial community; Coevolution; Cooccurrence network; Endophytic bacteria; Modularity

Indexed keywords

ALGA; ANOXIC SEDIMENT; COEVOLUTION; DEFENSE MECHANISM; GENOME; HOLISTIC APPROACH; HOMOLOGY; METABOLISM; MICROBIAL COMMUNITY; SYMPATRY;

MEDITERRANEAN SEA;

ALGAE; ANTHOZOA; BACTERIA (MICROORGANISMS); CAULERPA;

RNA 16S;

ANIMAL; ANTHOZOA; BACTERIUM; BIODIVERSITY; CAULERPA; ENDOPHYTE; GENETICS; MEDITERRANEAN SEA; MICROBIAL CONSORTIUM; MICROBIOLOGY; PLANT; SPECIES DIFFERENCE; SPONGE (PORIFERA);

ANIMALS; ANTHOZOA; BACTERIA; BIODIVERSITY; CAULERPA; ENDOPHYTES; MEDITERRANEAN SEA; MICROBIAL CONSORTIA; PLANTS; PORIFERA; RNA, RIBOSOMAL, 16S; SPECIES SPECIFICITY;

EID: 84949238895     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiv067     Document Type: Article

References (90)

1. Aires T, MarbàN, Serrao EA, et al. Selective elimination of chloroplastidial DNA for metagenomics of bacteria associated with the green alga Caulerpa Taxifolia (Bryopsidophyceae)1. J Phycol 2012;48:483-90
2. Aires T, Serrão EA, Kendrick G, et al. Invasion is a community affair: Clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa, track the invasion source. PLoS One 2013;8:e68429
3. Barbeŕan A, Bates ST, Casamayor EO, et al. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 2012;6:343-51
4. Barott KL, Rodriguez-Brito B, Janouskovec J, et al. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 2011;13:1192-204
5. Batagelj V, Mrvar A. Pajek - Analysis and visualization of large networks. Graph Drawing 2002;2265:477-8
6. Blondel VD, Guillaume J-L, Lambiotte R, et al. Fast unfolding of communities in large networks. J Stat Mech Theory E 2008;2008:P10008
7. Burke C, Thomas T, LewisM, et al. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 2011;5:590-600
8. Caporaso JG, Kuczynski J, Stombaugh J, et al. Correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 2010;7:335-6
9. Ceccherelli G, Cinelli F. Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. J Exp Mar Bio Ecol 1997;217:165-77
10. Chandler JA, Morgan Lang J, Bhatnagar S, et al. Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host-Microbe Model System. PLoS Genet 2011;7:e1002272, DOI:10.1371/journal.pgen.1002272
11. Chao A. Nonparametric estimation of the number of Classes in a population. Scand J Stat 1984;11:265-70
12. Chisholm JRM, Dauga C, Ageron E et al.'Roots' in mixotrophic algae. Nature 1996;381:382
13. Chisholm JRM, Fernex FE, Mathieu D, et al. Wastewater discharge, seagrass decline and algal proliferation on the Cote d'Azur. Mar Pollut Bull 1997;34:78-84
14. Chisholm JRM, Moulin P. Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 2003;48:787-94
15. Coenye T, Vandamme P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 2003;5:719-29
16. Costello E, Lauber C, Hamady M. Bacterial community variation in human body habitats across space and time. Science (80-) 2009;326:1694-7
17. Croft MT, Warren MJ, Smith AG. Algae need their vitamins. Eukaryot Cell 2006;5:1175-83
18. Crump BC, Koch EW. Attached bacterial populations shared by four species of aquatic angiosperms. Appl Environ Microb 2008;74:5948-57
19. Cś ardi G, Nepusz T. The igraph software package for complex network research. Inter Journal Complex Syst 2006;1695:1695
20. Dawes CJ, Lohr CA. Cvtoplasmic organization and endosymbiotic bacteria in the growing points of Caulerpa prolifera. Rev Algol 1978;13:309-14
21. Decker C, Olu K, Arnaud-Haond S, et al. Physical proximity may promote lateral acquisition of bacterial symbionts in vesicomyid clams. PLoS One 2013;8:e64830
22. Delbridge L, Coulburn J, Fagerberg W, et al. Community profiles of bacterial endosymbionts in four species of Caulerpa. Symbiosis 2004;37:335-44
23. Dittami SM, Eveillard D, Tonon T. A metabolic approach to study algal-bacterial interactions in changing environments. Mol Ecol 2014;23:1656-60
24. Egan S, Harder T, Burke C, et al. The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 2013;37:462-76
25. Elbeltagy A, Nishioka K, Sato T, et al. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microb 2001;67:5285-93
26. Faust K, Raes J. Microbial interactions: fromnetworks tomodels. Nat Rev Microbiol 2012;10:538-50.
27. Forster P, Torroni A, Renfrew C, et al. Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol Biol Evol 2001;18:1864-81
28. Gihring TM, Zhang G, Brandt CC, et al. A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer. Appl Environ Microb 2011;77:5955-65
29. Goecke F, Labes A, Wiese J, et al. Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 2010;409:267-99
30. Goffredi SK, Johnson SB, Vrijenhoek RC. Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microb 2007;73:2314-23
31. Haas BJ, Gevers D, Earl AM, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 2011;21:494-504
32. Hamel H. Quelques algues rares ou nouvelles pour la flore mediterraneenne. Bull Mus Nat Sci Nat 1926;32:420
33. Hammer Ø, Harper DAT, Ryan PD. Paleontological statistics software package for education and data analysis. Palaeontol Electron 2001;4:9-18
34. Handeler K, Wagele H, Wahrmund U, et al. Slugs' last meals: molecular identification of sequestered chloroplasts from different algal origins in Sacoglossa (Opisthobranchia, Gastropoda). Mol Ecol Resour 2010;10:968-78
35. Hollants J, Decleyre H, Leliaert F, et al. Life without a cell membrane: challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta). BMC Microbiol 2011;11:255
36. Hollants J, Leliaert F, De Clerck O, et al. What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiol Ecol 2013;83:1-16
37. Hollants J, Leliaert F, Verbruggen H, et al. Permanent residents or temporary lodgers: characterizing intracellular bacterial communities in the siphonous green alga Bryopsis. Proc Biol Sci 2013;280:20122659
38. Hollants J, Leroux O, Leliaert F, et al. Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 2011;6:e26458
39. Hollister EB, Engledow AS, Hammett AJM, et al. Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 2010;4:829-38
40. Holmer M, Marbà N, Lamote M, et al. Deterioration of sediment quality in seagrass meadows (Posidonia oceanica) invaded by macroalgae (Caulerpa sp.). Estuar Coast 2009;32:456-66
41. Huber JA, Mark Welch DB, Morrison HG, et al. Microbial population structures in the deep marine biosphere. Science 2007;318:97-100
42. Janson EM, Stireman JO, Singer MS, et al. Phytophagous insectmicrobe mutualisms and adaptive evolutionary diversification. Evolution 2008;62:997-1012
43. Jiao JY, Wang HX, Zeng Y, et al. Enrichment for microbes living in association with plant tissues. J Appl Microbiol 2006;100: 830-7
44. Joint I, Tait K, Wheeler G. Cross-kingdom signalling: exploitation of bacterial quorum sensingmolecules by the green seaweed Ulva. Philos T Roy Soc B 2007;362:1223-33
45. Keshtacher-Liebson E, Hadar Y, Chen Y. Oligotrophic bacteria enhance algal growth under iron-deficient conditions. Appl Environ Microb 1995;61:2439-41
46. Kirchman DL. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 2002;39:91-100
47. Kivelã M, Arnaud-Haond S, Saramãki J. EDENetworks: A userfriendly software to build and analyse networks in biogeography, ecology and population genetics. Mol Ecol Resour 2015;15:117-22
48. Krych L, Hansen CHF, Hansen AK, et al. Quantitatively different, yet qualitatively alike: a meta-analysis of themouse core gut microbiome with a viewtowards the human gutmicrobiome. PLoS ONE 2013;8:e62578
49. Kvennefors ECE, Sampayo E, Ridgway T, et al. Bacterial communities of two ubiquitous great barrier reef corals reveals both site-and species-specificity of common bacterial associates. PLoS One 2010;5:e10401, DOI:10.1371/journal.pone.0010401
50. Lachnit T, Blümel M, ImhoffJJF, et al. Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 2009;5:181-6
51. Lachnit T, Meske D, Wahl M, et al. Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 2011;13:655-65
52. Lancichinetti A, Fortunato S. Community detection algorithms: a comparative analysis. Phys Rev E 2009;80:056117
53. Langar H, Djellouli A, Ben Mustapha K, et al. Première signalisation de Caulerpa taxifolia (Vahl) C. Agardh en Tunisie. Bull Inst Sci Tech Mer 2000;27:7-8
54. Lee OO, Chui PY, Wong YH, et al. Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microb 2009;75:6147-56
55. Loudon AH, Woodhams DC, Parfrey LW, et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J 2014;8:830-40
56. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microb 2005;71:8228-35
57. Margulis L, Fester R. Symbiosis as a Source of Evolutionary Innovation. Cambridge, MA, USA: The MIT Press, 1992
58. Masson-Boivin C, Giraud E, Perret X, et al. Establishing nitrogenfixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 2009;17:458-66
59. Matsuo Y, Imagawa H, Nishizawa M, et al. Isolation of an algal morphogenesis. 2005;307:2005
60. Mechichi T, Stackebrandt E, Fuchs G. Alicycliphilus denitrificans gen. nov., sp. nov., a cyclohexanol-degrading, nitrate-reducing beta-proteobacterium. Int J Syst Evol Micr 2003;53:147-52
61. Meinesz A, Hesse B. Introduction et invasion de l'algue tropicale Caulerpa taxifolia enḾ editerrańee nord-occidentale. Oceanol Acta 1991;14:415-26
62. Meusnier I, Olsen JL, Stam WT, et al. Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 2001;10:931-46
63. Moalic Y, Desbruyères D, Duarte CM, et al. Biogeography revisited with network theory: retracing the history of hydrothermal vent communities. Syst Biol 2012;61:127-37
64. Moore AM, Munck C, Sommer MO, et al. Functional metagenomic investigations of the human intestinal microbiota. Front Microbiol 2011;2:1-8
65. Myshrall KL, Mobberley JM, Green SJ, et al. Biogeochemical cycling and microbial diversity in the thrombolitic microbialites of Highborne Cay, Bahamas. Geobiology 2010;8: 337-54
66. Nakanishi K, Nishijima M. Bacteria that induce morphogenesis in Ulva pertusa (chlorophyta). 1996;32:479-82
67. Newman M. The structure and function of complex networks. SIAM Rev 2003;45:167-256
68. Newman MEJ. Finding community structure in networks using the eigenvectors of matrices. Phys Rev E 2006;74: 036104
69. Orole O, Adejumo T. Bacterial and fungal endophytes associated with grains and roots of maize. J Ecol Nat Environ 2011;3:298-303
70. Panayotidis P. On the enigmatic origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Mediterr Mar Sci 2006;7:119-21
71. Pérez-Ruzafa A, Marcos C, Bernal CM, et al. Cymodocea nodosa vs. Caulerpa prolifera: causes and consequences of a long term history of interaction in macrophyte meadows in the mar Menor coastal lagoon (Spain, Southwestern Mediterranean). Estuar Coast Shelf S 2012;110:101-15
72. Price MN, Dehal PS, Arkin AP. FastTree 2-Approximately maximum-likelihood trees for large alignments. PLoS One 2010;5:e9490, DOI:10.1371/journal.pone.0009490
73. Polzin T, Daneschmand SV. On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 2003;31:12-20.
74. Rayss T. Sur les Caulerpes de la cote palestinienne. Palest J Bot Jerus Ser 1941;2:103-24
75. Reichenbach H. Order I. Cytophagales Leadbetter 1974, 99AL. In: Staley JT, Bryant MP, Pfennig N et al. (ed). Bergey's Manual of Systematic Bacteriology. Baltimore, MD:Williams Wilkins 1989;3:2011-3
76. Reshef L, Koren O, Loya Y, et al. The coral probiotic hypothesis. Environ Microbiol 2006;8:2068-73
77. Rosenberg E, Koren O, Reshef L, et al. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 2007;5:355-62
78. Rosvall M, Bergstrom CT. Community structure in directed networks. P Natl Acad Sci USA 2008;105:1118-23
79. Sachs JL, Skophammer RG, Regus JU. Evolutionary transitions in bacterial symbiosis. P Natl Acad Sci USA 2011;108(Suppl):10800-7
80. Schmitt S, Tsai P, Bell J, et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 2012;6:564-76
81. Stewart FJ, Young CR, Cavanaugh CM. Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol Biol Evol 2008;25:673-87
82. Tonon T, Eveillard D, Prigent S, et al. Toward systems biology in brown algae to explore acclimation and adaptation to the shore environment. OMICS 2011;15:883-92
83. Tujula NA, Crocetti GR, Burke C, et al. Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 2010;4:301-11
84. Turnbaugh PJ, Ridaura VK, Faith JJ, et al. Metagenomic analysis in humanized gnotobiotic mice. 2010;1:1-19
85. Verlaque M, Boudouresque CF, Meinesz A, et al. The Caulerpa racemosa complex (Caulerpales, Ulvophyceae) in the Mediterranean Sea. Bot Mar 2000;43:49-68
86. Wakelin SA, ColloffMJ, Kookana RS. Effect of wastewater treatment plant effluent on microbial function and community structure in the sediment of a freshwater stream with variable seasonal flow. Appl Environ Microb 2008;74: 2659-68
87. Wang Q, Garrity GM, Tiedje JM, et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 2007;73:5261-7
88. Weinberger F, Beltran J, Correa JA, et al. Spore release in Acrochaetium sp. (Rhodophyta) is bacterially controlled. J Phycol 2007;43:235-41
89. Wiese J, Thiel V, Gartner A, et al. Kiloniella laminariae gen. nov., sp. nov., an alphaproteobacterium from the marine macroalga Laminaria saccharina. Int J Syst Evol Micr 2009;59:350-6
90. Zilber-Rosenberg I, Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 2008;32:723-35.