Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 522:98–101

    CAS  PubMed  Google Scholar 

  • 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 13:1192–1204

    CAS  PubMed  Google Scholar 

  • Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83

    Google Scholar 

  • 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 182:317–324

    Google Scholar 

  • Borkow G, Gabbay J (2005) Copper as a biocidal tool. Curr Med Chem 12:2163–2175

    CAS  PubMed  Google Scholar 

  • 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 51:472–484

    CAS  Google Scholar 

  • 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. https://doi.org/10.1093/femsec/fiw110

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 38:321–326

    CAS  Google Scholar 

  • 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 492–521

    Google Scholar 

  • 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 108:14288–14293

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1016/j.jhin.2018.05.013

    Article  Google Scholar 

  • 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 271

    Google Scholar 

  • 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. https://doi.org/10.3389/fmicb.2015.00230

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 8:52–62

    CAS  PubMed  Google Scholar 

  • 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 11:463–472

    Google Scholar 

  • 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 94:94–102

    CAS  PubMed  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    CAS  PubMed  Google Scholar 

  • Dafforn KA, Lewis JA, Johnston EL (2011) Antifoulings strategies: history and regulation, ecological impacts and mitigation. Mar Pollut Bull 62:365–453

    Google Scholar 

  • Delbridge L, Coulburn J, Facerberg W, Tisa LS (2004) Community profiles of bacterial endosymbionts in four species of Caulerpa. Symbiosis 37:335–344

    CAS  Google Scholar 

  • 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 40:370–382

    CAS  PubMed  Google Scholar 

  • 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 105:80–89

    PubMed  Google Scholar 

  • Egan S, Herder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462–476

    CAS  PubMed  Google Scholar 

  • Farias DR, Hurd CL, Eriksen RS, Macleod CK (2018) Macrophytes as bioindicators of heavy metal pollution in estuarine and coastal environments. Mar Pollut Bull 128:175–184

    CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0027387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fries L (1993) Vitamine B12 heterotrophy in Fucus spiralis and Ascophyllum nodosum (Fucales, Phaeophyta) in axenic cultures. Bot Mar. 36:5–7

    CAS  Google Scholar 

  • 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. https://doi.org/10.3390/md14050100

    Article  CAS  PubMed Central  Google Scholar 

  • Gachon C, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15:633–640

    CAS  PubMed  Google Scholar 

  • 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 48:47–60

    Google Scholar 

  • 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 54:195–199

    CAS  Google Scholar 

  • Head WD, Carpenter EJ (1975) Nitrogen fixation associated with the marine macroalga Codium fragile. Limnol Oceanogr 20:815–823

    CAS  Google Scholar 

  • Hentschel U, Piel J, Degnam SM, Taylor MW (2012) Genomic insights into marine sponge microbiome. Nat Rev Microbiol 10:641–654

    CAS  PubMed  Google Scholar 

  • Ho YB (1990) Ulva lactuca as a bioindicator of metal contamination in intertidal waters in Hong Kong. Hydrobiologia 203:73–81

    CAS  Google Scholar 

  • 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:e26458

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 280:20122659

    Google Scholar 

  • 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 24:525–534

    Google Scholar 

  • 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 20:183–190

    CAS  Google Scholar 

  • 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 16:1466–1476

    Google Scholar 

  • 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 69:95–105

    CAS  Google Scholar 

  • 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 121:286–292

    CAS  PubMed  Google Scholar 

  • Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr Opin Biotechnol 33:125–129

    CAS  PubMed  Google Scholar 

  • Lachnit T, Blümel M, Imhoff J, Wahl M (2011) Specific epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665

    Google Scholar 

  • 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 2:212–222

    Google Scholar 

  • 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 39:1384–1386

    PubMed  PubMed Central  Google Scholar 

  • Martin M, Portelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98:2817–2935

    Google Scholar 

  • 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 6:1487

    PubMed  PubMed Central  Google Scholar 

  • Mato Rodriguez L, Alatossava T (2010) Effects of coper on germination, growth and sporulation of Clostridium tyrobutyricum. Food Microbiol 27:434–437

    CAS  PubMed  Google Scholar 

  • 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 5:25–35

    CAS  PubMed  Google Scholar 

  • 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 33:904–916

    CAS  PubMed  Google Scholar 

  • 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 10:931–946

    CAS  PubMed  Google Scholar 

  • 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 13:487

    Google Scholar 

  • Paracelsus (1538) Dritte defensio

  • Reed RH, Moffat L (1982) Copper toxicity and copper tolerance in Enteromorpha compressa (L.) Grev. J. Exp. Mar. Biol. Ecol. 69:85–103

    Google Scholar 

  • Riley JP (1966) In: Riley JP, Skirrow GS (eds) Chemical oceanography tome 2. Academic Press, London, pp 323–384

    Google Scholar 

  • Rios M, Nieto JJ, Ventosa A (1998) Numerical taxonomy of heavy metal-tolerant nonhalophilc bacteria from hypersaline environments. Int Microbiol 1:45–51

    CAS  PubMed  Google Scholar 

  • Rosenberg G, Paerl HW (1981) Nitrogen fixation by blue-green algae associated with siphonous green seaweed Codium decorticatum: effects on ammonium uptake. Mar Biol 61:151–158

    Google Scholar 

  • Rosenberg E, Zilbner-Rosenberg I (2018) The hologenome concept of evolution after 10 years. Microbiome 6:78. https://doi.org/10.1186/s40168-018-0457-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan S, McLoughlin P, O’Donovan O (2012) A comprehensive study of metal distribution in three main classes of seaweeds. Environ Pollut 167:171–177

    CAS  PubMed  Google Scholar 

  • 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 7:1–10

    Google Scholar 

  • 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 80:1758–1770

    PubMed  Google Scholar 

  • Sambrook J, Frotsch EF, Maniatis T (1987) Molecular cloning: a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p 1626

    Google Scholar 

  • Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyl-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331–355

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 44:1565–1571

    CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1128/mBio.01980-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:301–311

    PubMed  Google Scholar 

  • 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 128:431–437

    Google Scholar 

  • Weaver L, Michels HT, Keevil CW (2007) Survival of Clostridium difficile on coper and steel: futuristic options for hospital hygiene. J Hosp Infect 68:145–151

    Google Scholar 

  • 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 11:287–300

    CAS  Google Scholar 

  • 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. 387:320–332

    CAS  Google Scholar 

  • 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 606:135–150

    CAS  PubMed  Google Scholar 

  • 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 252:264–276

    Google Scholar 

  • 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 30:200–205

    CAS  Google Scholar 

  • Zilbner-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735

    Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Laboratoire de Biotechnologie et de Chimie Marines – IUEM. Skol-Veur Kreisteiz Breizh - UBS, BP 92116, 56321, Lorient, Brittany, France

    Gaël Le Pennec

  2. Laboratoire de l’Environnement Marin – UMR 6539, IUEM University of Brest, 29280, Plouzané, Brittany, France

    Erwan Ar Gall

Authors
  1. Gaël Le Pennec
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erwan Ar Gall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gaël Le Pennec.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Le Pennec, G., Gall, E.A. The microbiome of Codium tomentosum: original state and in the presence of copper. World J Microbiol Biotechnol 35, 167 (2019). https://doi.org/10.1007/s11274-019-2740-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-019-2740-8

Keywords

Search

Navigation