The microbiome of Codium tomentosum: original state and in the presence of copper

  • Gaël Le PennecEmail author
  • Erwan Ar Gall
Original Paper


Codium tomentosum, as all organisms, hosts transiently and permanently numerous microorganisms. These holobionts can undergo environmental pressures influencing both partners creating modifications/imbalances within the associations, which may directly influence their physiological status by selecting tolerant bacteria. Furthermore, the capability of remediation of the associated bacterioflora, in particular of metallic trace elements, may provide the host with survival potential in polluted environments. In this context, we incubated C. tomentosum thalli in the presence of copper and studied its influence on the reference bacteriome. Whatever the concentration of copper, no shift was evidenced on the bacteriome at the phylum level. However, a high copper concentration enriched the bacteriome of C. tomentosum in both the genera Clostridium and Pseudolteromonas.


Codium tomentosum Copper Microbiome Holobiont 



The authors would like to thank the Institut Universitaire Européen de la Mer (Plouzané – Brittany, France) for its financial support and Agrocampus Ouest site Beg-Meil (Beg-Meil, Brittany, France) which allowed the access to its zootechnic installations where took place the experimental procedure. Noémie Potineau and Clément Toletti are thanked for their technical assistance.


  1. Amin SA, Hmelo LR, Van Tol HM, Duran BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signaling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101PubMedGoogle Scholar
  2. Barott KL, Rodroguez-Brito B, Janouskovec J, Marhaver KL, Smith JE, Keelin P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and a reef-building coral Montastreae annularis. Environ Microbiol 13:1192–1204PubMedGoogle Scholar
  3. Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83Google Scholar
  4. Benkad A, Laissaoui A, Tornero MA, Benmansour M, Chakir E, Garrido IM, Moreno JB (2011) Trace metals and radionucleides in macroalgae from Moroccan coastal waters. Environ Monit Assess 182:317–324Google Scholar
  5. Borkow G, Gabbay J (2005) Copper as a biocidal tool. Curr Med Chem 12:2163–2175PubMedGoogle Scholar
  6. Boubonari T, Malea P, Kevrekidis T (2008) The green seaweed Ulva rigida as a bioindicator of metals (Zn, Cu, Pb and Cd) in a low-salinity coastal environment. Bot Mar 51:472–484Google Scholar
  7. Brodie J, Williamson C, Barker GL, Walker RH, Briscoe A, Yallop M (2016) Characterizing the microbiome of Corallina officinalis, a dominant calcified intertidal red alga. FEMS Microbiol Ecol. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brooks RP, Presley BJ, Kaplan IR (1967) Determination of copper in saline waters by atomic absorption spectrophotometry combined with apdc-mibk extraction. Anal Chim Acta 38:321–326Google Scholar
  9. Brooks S, Waldock M (2009) The use of copper as a biocide in marine antifouling paints. In: Hellio C, Woodhead YD (eds) Advances in marine antifouling coatings and technologies. Cambridge Publishing Limited, London, pp 492–521Google Scholar
  10. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108:14288–14293PubMedGoogle Scholar
  11. Butler JP (2018) Effect of copper-impregnated composite bed linens and patient grown on healthcare-associated infection rates in six hospitals. J. Hosp. Infect. 5:6. CrossRefGoogle Scholar
  12. Cabioc’h J, Floc’h JY, Le Toquin A, Boudouresque CF, Meinesz A, Verlaque M (2014) Algues des mers d’Europe. Guide Delachaux, Delachaux et Niestlé, Paris, p 271Google Scholar
  13. Campbell AH, Marzinellei AM, Geber J, Steinberg PD (2015) Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front Microbiol 6:230. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cavalcanti GS, Gregoracci GB, Dos Santos EO, Silveira CB, Meirelles PM, Gotoh K, Nakamura S, Lida T, Sawabe T, Rezende CE, Francini-Filho RB, Moura RL, Amado-Filho GM, Thompson FL (2014) Physiologic and metagenomics attributes of the rhodoliths forming the largest CaCO3 bed in the South Atlantic Ocean. ISME J 8:52–62PubMedGoogle Scholar
  15. Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (1999) Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 11:463–472Google Scholar
  16. Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses of copper-induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94:94–102PubMedGoogle Scholar
  17. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93PubMedGoogle Scholar
  18. Dafforn KA, Lewis JA, Johnston EL (2011) Antifoulings strategies: history and regulation, ecological impacts and mitigation. Mar Pollut Bull 62:365–453Google Scholar
  19. Delbridge L, Coulburn J, Facerberg W, Tisa LS (2004) Community profiles of bacterial endosymbionts in four species of Caulerpa. Symbiosis 37:335–344Google Scholar
  20. Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R, Simon M, Brinkoff T (2017) Rhodobacteraceae on the marine brown alga Fucus spiralis are abundant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol 40:370–382PubMedGoogle Scholar
  21. Dos Santos RW, Schmidt EC, Felix De L, MR, Polo LK, Kreusch M, Pereira DT, Costa GB, Simioni C, Chow F, Ramlov F, Maraschin M, Bouzon ZL, (2014) Bioabsorption of cadmium, copper and lead by the red macroalga Gelidium floridanum: physiological responses and ultrastructure features. Ecotoxicol Environ Saf 105:80–89PubMedGoogle Scholar
  22. Egan S, Herder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462–476PubMedGoogle Scholar
  23. Farias DR, Hurd CL, Eriksen RS, Macleod CK (2018) Macrophytes as bioindicators of heavy metal pollution in estuarine and coastal environments. Mar Pollut Bull 128:175–184PubMedGoogle Scholar
  24. Fernandes N, Case RJ, Longford SR, Seyedsayamdost MR, Steinberg PD, Kjelleberg S, Thomas T (2011) Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red algae Delisea pulchra. PLoS ONE 6(12):e27387. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fries L (1993) Vitamine B12 heterotrophy in Fucus spiralis and Ascophyllum nodosum (Fucales, Phaeophyta) in axenic cultures. Bot Mar. 36:5–7Google Scholar
  26. Fuentes JL, Garbayo I, Cuaresma M, Montero Z, Gonzalez-del-Valle M, Vilchez C (2016) Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar Drugs 14:100. CrossRefPubMedCentralGoogle Scholar
  27. Gachon C, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15:633–640PubMedGoogle Scholar
  28. Goecke F, Labes A, Wiese J, Imhoff JF (2013) Phylogenetic analysis and antibiotic activity of bacteria isolated from the surface of two co-occurring macroalgae from the Baltic Sea. Eur J Phycol 48:47–60Google Scholar
  29. Hall A, Fielding AH, Butler M (1979) Mechanisms of copper tolerance in the marine fouling alga Ectocarpus siliculosus: evidence for an exclusion mechanism. Mar Biol 54:195–199Google Scholar
  30. Head WD, Carpenter EJ (1975) Nitrogen fixation associated with the marine macroalga Codium fragile. Limnol Oceanogr 20:815–823Google Scholar
  31. Hentschel U, Piel J, Degnam SM, Taylor MW (2012) Genomic insights into marine sponge microbiome. Nat Rev Microbiol 10:641–654PubMedGoogle Scholar
  32. Ho YB (1990) Ulva lactuca as a bioindicator of metal contamination in intertidal waters in Hong Kong. Hydrobiologia 203:73–81Google Scholar
  33. Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A (2011) Who is in there? exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 6:e26458PubMedPubMedCentralGoogle Scholar
  34. Hollants J, Leliaert F, Verbruggen H, Willems A, De Clerck O (2013) Permanent residents or temporary lodgers: characterizing intracellular bacterial communities in the siphonous green alga Bryopsis. Proc R Soc B Biol Sci 280:20122659Google Scholar
  35. Ismail-Ben Ali A, El Bour M, Ktari L, Bolhuis H, Ahmed M, Boudabbous A, Stal LJ (2011) Jania rubens-associated bacteria: molecular identification and antimicrobial activity. J Appl Phycol 24:525–534Google Scholar
  36. Kang YH, Shin JA, Kim MS, Chung IK (2008) A preliminary study of the bioremediation potential of Codium fragile applied to seaweed integrated multi-trophic aquaculture (IMTA) during the summer. J Appl Phycol 20:183–190Google Scholar
  37. Kazamia E, Czesnick H, Nguyen TT, Croft MT, Sherwood E, Sasso S, Hodson SJ, Warren MJ, Smith AG (2012) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 16:1466–1476Google Scholar
  38. Kim BH, Kang Z, Ramanan R, Choi JE, Cho DH, Oh HM, Kim HS (2014) Role of rhizobium, a plant growth promoting bacterium, in enhancing algal biomass through mutualistic interaction. Biomass Bioenergy 69:95–105Google Scholar
  39. Kita A, Miura T, Kawata S, Yamaguchi T, Okamura Y, Aki T, Matsumura Y, Tajima T, Kato J, Nishio N, Nakashimada Y (2016) Bacterial community structure and predicted alginate metabolic pathway in alginate-degrading bacterial consortium. J Biosci Bioeng 121:286–292PubMedGoogle Scholar
  40. Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr Opin Biotechnol 33:125–129PubMedGoogle Scholar
  41. Lachnit T, Blümel M, Imhoff J, Wahl M (2011) Specific epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665Google Scholar
  42. Le Chevanton M, Garnier M, Bougaran G, Schreiber N, Lukomska E, Bérard JB, Fouilland E, Bernard O, Cadoret JP (2013) Screening and selection of growth-promoting bacteria for Dunaliella cultures. Algal Res 2:212–222Google Scholar
  43. Madden GR, Heon BE, Sifri CD (2018) Effect of copper-impregnated linens on multidrug-resistant organism acquisition and Clostridium difficile infection at a long-term accurate-care hospital. Infect Control Hosp Epidemiol 39:1384–1386PubMedGoogle Scholar
  44. Martin M, Portelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98:2817–2935Google Scholar
  45. Martin M, Barbeyron T, Martin R, Portetelle D, Michel G, Vandenbol M (2015) The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol 6:1487PubMedPubMedCentralGoogle Scholar
  46. Mato Rodriguez L, Alatossava T (2010) Effects of coper on germination, growth and sporulation of Clostridium tyrobutyricum. Food Microbiol 27:434–437PubMedGoogle Scholar
  47. Matsuo Y, Suzuki M, Kasai H, Shizuri Y, Harayama S (2003) Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum. Environ Microbiol 5:25–35PubMedGoogle Scholar
  48. McElroy DJ, Hichuli DF, Doblin MA, Murphy RJ, Blackburn RJ, Coleman RA (2017) Effect of copper on multiple successional stages of a marine fouling assemblage. Biofouling 33:904–916PubMedGoogle Scholar
  49. Meusnier I, Olsen JL, Stam WT, Destombe C, Valero M (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provides clues to the origin of the Mediterranean introduction. Mol Ecol 10:931–946PubMedGoogle Scholar
  50. Oliveira LS, Gregoracci GB, Silva GGZ, Salgado LT, Filho AG, Alves-Ferreira M, Pereira RC, Thompson FL (2012) Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genom 13:487Google Scholar
  51. Paracelsus (1538) Dritte defensioGoogle Scholar
  52. Reed RH, Moffat L (1982) Copper toxicity and copper tolerance in Enteromorpha compressa (L.) Grev. J. Exp. Mar. Biol. Ecol. 69:85–103Google Scholar
  53. Riley JP (1966) In: Riley JP, Skirrow GS (eds) Chemical oceanography tome 2. Academic Press, London, pp 323–384Google Scholar
  54. Rios M, Nieto JJ, Ventosa A (1998) Numerical taxonomy of heavy metal-tolerant nonhalophilc bacteria from hypersaline environments. Int Microbiol 1:45–51PubMedGoogle Scholar
  55. Rosenberg G, Paerl HW (1981) Nitrogen fixation by blue-green algae associated with siphonous green seaweed Codium decorticatum: effects on ammonium uptake. Mar Biol 61:151–158Google Scholar
  56. Rosenberg E, Zilbner-Rosenberg I (2018) The hologenome concept of evolution after 10 years. Microbiome 6:78. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ryan S, McLoughlin P, O’Donovan O (2012) A comprehensive study of metal distribution in three main classes of seaweeds. Environ Pollut 167:171–177PubMedGoogle Scholar
  58. Saez CA, Lobos MG, Macaya EC, Oliva D, Quiroz W, Brown MT (2012) Variation in patterns of metal accumulation in thallus parts of Lessonia trabeculata (Laminariales; Pheophyceae): implications for biomonitoring. PLoS ONE 7:1–10Google Scholar
  59. Salaün S, Kervarec N, Potin P, Haras D, Piotto M, La Barre S (2010) Whole-cell spectroscopy is a convenient tool to assist molecular identification of cultivable marine bacteria and to investigate their adaptive metabolism. Talanta 80:1758–1770PubMedGoogle Scholar
  60. Sambrook J, Frotsch EF, Maniatis T (1987) Molecular cloning: a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p 1626Google Scholar
  61. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyl-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331–355PubMedPubMedCentralGoogle Scholar
  62. Sifri CD, Burke GH, Enfield KB (2016) Reduced health care-associated infections in an acute care community hospital using a combination of self-disinfecting copper-impregnated composite hard surfaces and linens. Am J infect Control 44:1565–1571PubMedGoogle Scholar
  63. Tian RM, Wang Y, Bougouffa S, Gao ZM, Cai L, Zhang WP, Bajic V, Qian PY (2014) Effect of copper treatment on the composition and function of the bacterial community in the sponge Halichondria cymaeformis. MBio. 5:e01980. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmström C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with the green marine Ulvacean alga. ISME J 4:301–311PubMedGoogle Scholar
  65. Van der Wal H, Sperber BLHM, Houweling-Tan B, Bakker RRC, Brandenburg W, Lopez-Contreras AM (2016) Production of acetone, butanol, and ethanol from biomass of the green seaweed Ulva lactuca. Bioresour Technol 128:431–437Google Scholar
  66. Weaver L, Michels HT, Keevil CW (2007) Survival of Clostridium difficile on coper and steel: futuristic options for hospital hygiene. J Hosp Infect 68:145–151Google Scholar
  67. Wiese J, Thiel V, Nage K, Staufenberger T, Imhoff JF (2009) Diversity of antibiotic-active bacteria associated with the brown algae Laminaria saccharina from the Baltic Sea. Mar Biotechnol 11:287–300Google Scholar
  68. Zbikowski R, Szefer P, Latala A (2007) Comparison of green algae Cladophora sp. and Enteromorpha sp. as potential biomonitors of chemical elements in southern Baltic. Sci Tot Environ. 387:320–332Google Scholar
  69. Zhou Q, Zhang J, Fu J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150PubMedGoogle Scholar
  70. Zhou Y, Yang H, Hu H, Liu Y, Mao Y, Zhou H, Xu X, Zhang F (2006) Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 252:264–276Google Scholar
  71. Zhou WZ, Li WW, Zhang YZ, Gao BY, Wang J (2009) Biosorption of Pb2+ and Cu2+ by an exopolysaccharide from the deep-sea psychrophilic bacterium Pseudoalteromonas sp. SM9913. Huang Jing Ke Xue 30:200–205Google Scholar
  72. Zilbner-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratoire de Biotechnologie et de Chimie Marines – IUEM. Skol-Veur Kreisteiz Breizh - UBSLorientFrance
  2. 2.Laboratoire de l’Environnement Marin – UMR 6539IUEM University of BrestPlouzanéFrance

Personalised recommendations