Advertisement

Journal of Applied Phycology

, Volume 31, Issue 2, pp 867–883 | Cite as

Potential interactions bacteria-brown algae

  • Michelle Marchezan F. de MesquitaEmail author
  • Mirian A. C. Crapez
  • Valéria L. Teixeira
  • Diana N. Cavalcanti
VI REDEALGAS WORKSHOP (RIO DE JANEIRO, BRAZIL)

Abstract

Macroalgae play a crucial role in marine ecosystems when they contribute to the global primary production in the habitats formation, providing food and shelter to a range of aquatic organisms. They have a number of interactions with bacteria and other organisms such as fouling and disease. To inhibit the settling, growing, and biofilm formation by bacteria, it has been suggested that the macroalgae influence bacterial metabolism and quorum sensing through the production of secondary metabolites with antibiotic effect. Macroalgae-bacteria interactions have been investigated for many years. These interactions can be beneficial when the bacteria assist with the normal development of macroalgae as well as reducing secondary fouling on the algal surface. On the other hand, the interactions may have a deleterious effect when the biofilm impairs the photosynthetic ability or promotes disease development. This review reports the recent advances in the understanding of bacteria-brown algae interactions, highlighting the diversity and functional role of epiphytic bacteria, including the maintenance of the health of the algae and the biological activities described from this association. Through combined bacterial culture, microscopy, and molecular biology, it has been possible to identify and establish the phylogenetic origin of different bacterial communities associated with brown algae, being predominantly the phyla Proteobacteria, Bacteroidetes, and Firmicutes. Further investigation of the bacterial communities that live on different macroalgae using new technologies are still required, mainly to evaluate the production and secretions of metabolites with biotechnological potential.

Keywords

Secondary metabolites Biofilms Microbial ecology Biological activity Chemical interaction 

Notes

Acknowledgements

The first author is thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) for the PhD fellowship. This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). The authors also thank the collaboration of MSc. Ana Débora Nunes Pinheiro in the review of English and suggestions for this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2018_1573_MOESM1_ESM.docx (37 kb)
ESM 1 (DOCX 36 kb)
10811_2018_1573_MOESM2_ESM.docx (38 kb)
ESM 2 (DOCX 38 kb)

References

  1. Abdel-Raouf N, Mohamed HM, Mostafa SS, Ibraheem IBM (2017) Controlling of microbial growth by using Cystoseira barbata extract. Egypt J Bot 57:469–477Google Scholar
  2. Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240CrossRefPubMedGoogle Scholar
  3. Aires T, Serrão EA, Kendrick G, Duarte CM, Arnaud-Haond S (2013) Invasion is a community affair: clandestine followers in the bacterial community associated to green algae, Caulerpara racemosa, track the invasion source. PLoS One 8(7): e68429Google Scholar
  4. Akbari V, Zafari S, Yegdaneh A (2018) Anti-tuberculosis and cytotoxic evaluation of the seaweed Sargassum boveanum. Res Pharm Sci 13:30–37CrossRefPubMedPubMedCentralGoogle Scholar
  5. Akremi N, Cappoen D, Anthonissen R, Verschaeve L, Bouraoui A (2017) Phytochemical and in vitro antimicrobial and genotoxic activity in the brown algae Dictyopteris membranacea. S Afr J Bot 108:308–314CrossRefGoogle Scholar
  6. Albakosh MA, Naidoo RK, Kirby B, Bauer R (2016) Identification of epiphytic bacterial communities associated with the brown alga Splachnidium rugosum. J Appl Phycol 28:1891–1901CrossRefGoogle Scholar
  7. Ali AIB, Bour ME, Ktari L, Bolhuis H, Ahmed M, Boudabbous A, Stal LJ (2012) Jania rubens-associated bacteria: molecular identification and antimicrobial activity. J Appl Phycol 24:525–534CrossRefGoogle Scholar
  8. Ali SS, Shaaban MT, Abomohra AEF, El-Safity K (2016) Macroalgal activity against multiple drug resistant Aeromonas hydrophila: a novel treatment study towards enhancement of fish growth performance. Microb Pathog 101:89–95CrossRefPubMedGoogle Scholar
  9. Al-Saif SSA, Raouf NA, El-Wazanani HA, Aref IA (2014) Antibacterial substances from marine algae isolated from Jeddah coast of Red Sea, Saudi Arabia. Saudi J Biol Sci 21:57–64CrossRefPubMedGoogle Scholar
  10. Alvarado P, Huang Y, Wang J, Garrido I, Leiva S (2018) Phylogeny and bioactivity of epiphytic gram-positive bacteria isolated from three co-occurring Antarctic macroalgae. Antonie Van Leeuwenhoek.  https://doi.org/10.1007/s10482-018-1044-6
  11. Alves RCC, Mercês PFF, Souza IRA, Almeida CMA, Silva APS, Lima VLM, Correia MTS, Silva MV, Silva AG (2016) Antimicrobial activity of seaweeds of Pernambuco, northeastern coast of Brazil. Afr J Microbiol Res 10:312–318CrossRefGoogle Scholar
  12. Andersen RA (2004) Biology and systematics of heterokont and haptophyte algae. Am J Bot 91:1508–1522CrossRefPubMedGoogle Scholar
  13. Armstrong E, Yan L, Boyd KG, Wright PC, Burgess JG (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 46:37–40CrossRefGoogle Scholar
  14. Bai AJ, Rai VR (2011) Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf 10:183–193CrossRefGoogle Scholar
  15. Balakirev ES, Krupnova TN, Ayala FJ (2012) Symbiotic associations in the phenotypically-diverse brown alga Saccharina japonica. PLoS One 7(6):e39587CrossRefPubMedPubMedCentralGoogle Scholar
  16. Barbeyron T, L’Haridon S, Michel G, Czjzek M (2008) Mariniflexile fucanivorans sp. nov., a marine member of the Flavobacteriaceae that degrades sulphated fucans from brown algae. Int J Syst Evol Microbiol 58:2107–2113CrossRefPubMedGoogle Scholar
  17. Barott KL, Rodriguez-Brito B, Janouskovec J, Marhaver KL, Smith JE, Keeling P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192–1204CrossRefPubMedGoogle Scholar
  18. Batista D, Carvalho AP, Costa R, Coutinho R, Dobretsov S (2014) Extracts of macroalgae from the Brazilian coast inhibit bacterial quorum sensing. Bot Mar 57:441–447CrossRefGoogle Scholar
  19. Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on kelp (Laminaria hyperborea). Aquat Microb Ecol 60:71–83CrossRefGoogle Scholar
  20. Bengtsson MM, Sjøtun K, Lanzén A, Øvreås L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188–2198CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bogolitsyn KG, Kaplitsin PA, Dobrodeeva LK, Druzhinina AS, Ovchinnikov DV, Parshina AE, Shulgina EV (2017) Fatty acid composition and biological activity of supercritical extracts from arctic brown algae Fucus vesiculosus. Russ J Phys Chem B 11:1144–1152CrossRefGoogle Scholar
  22. Bondoso J, Balagué V, Gasol JM, Lage OM (2013) Community composition of the Planctomycetes associated with different macroalgae. FEMS Microbiol Ecol 88:445–456CrossRefGoogle Scholar
  23. Bondoso J, Godoy-Vitorino F, Balagué V, Gasol JM, Harder J, Lage OM (2017) Epiphytic Planctomycetes communities associated with three main groups of macroalgae. FEMS Microbiol Ecol 93(3):fiw255.  https://doi.org/10.1093/femsec/fiw255
  24. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011a) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600CrossRefPubMedGoogle Scholar
  25. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011b) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci U S A 108:14288–14293CrossRefPubMedPubMedCentralGoogle Scholar
  26. Busetti A, Shaw G, Megaw J, Gorman SP, Maggs CA, Gilmore BF (2015) Marine derived quorum sensing inhibitory activities enhance the antibacterial efficacy of tobramycin against Pseudomonas aeruginosa. Mar Drugs 13:1–28CrossRefGoogle Scholar
  27. Campbell AH, Marzinelli EM, Gelber J, Steinberg PD (2015) Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front Microbiol 6:230CrossRefPubMedPubMedCentralGoogle Scholar
  28. Carvalho AP, Batista D, Dobretsov S, Coutinho R (2017) Extracts of seaweeds as potential inhibitors of quorum sensing and bacterial growth. J Appl Phycol 29:789–797CrossRefGoogle Scholar
  29. Cavalcanti DN, Rezende CM, Pinto AC, Teixeira VL (2006) Diterpenoid constituents from the brown alga Dictyota menstrualis (Dictyotaceae, Phaeophyta). Nat Prod Comm 1:609–611Google Scholar
  30. Chakraborty K, Thilakan B, Chakraborty RD, Raola VK, Joy M (2017) O-heterocyclic derivatives with antibacterial properties from marine bacterium Bacillus subtilis associated with seaweed, Sargassum myriocystum. Appl Microbiol Biotechnol 101:569–583CrossRefPubMedGoogle Scholar
  31. Chakraborty K, Thilakan B, Kizhakkekalam VK (2018) Antibacterial aryl-crowned polyketide from Bacillus subtilis associated with seaweed Anthophycus longifolius. J Appl Microbiol 124:108–125CrossRefPubMedGoogle Scholar
  32. Cock JM, Peters AF, Coelho SM (2011) Brown algae. Curr Biol 21:R573–R575CrossRefPubMedGoogle Scholar
  33. Coelho-Souza SA, Jenkins SR, Casarin A, Baeta-Neves MH, Salgado LT, Guimaraes JRD, Coutinho R (2017) The effect of light on bacterial activity in a seaweed holobiont. Microb Ecol 74:868–876CrossRefPubMedGoogle Scholar
  34. Coste O, Malta EJ, López JC, Fernández-Díaz C (2015) Production of sulfated oligosaccharides from the seaweed Ulva sp. using a new ulvan-degrading enzymatic bacterial crude extract. Algal Res 10:224–231CrossRefGoogle Scholar
  35. Cox S, Abu-Ghannam N, Gupta S (2010) An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int Food Res J 17:205–220Google Scholar
  36. Cray JA, Bell ANW, Bhaganna P, Mswaka AY, Timson DJ, Hallsworth JE (2013) The biology of habitat dominance; can microbes behave as weeds? Microb Biotechnol 6:453–492CrossRefPubMedPubMedCentralGoogle Scholar
  37. Dang H, Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66:467–475CrossRefPubMedPubMedCentralGoogle Scholar
  38. De Corato U, Salimbeni R, De Pretis A, Avella N, Patruno G (2017) Antifungal activity of crude extracts from brown and red seaweeds by a supercritical carbon dioxide technique against fruit postharvest fungal diseases. Postharvest Biol Technol 131:16–30CrossRefGoogle Scholar
  39. Del Olmo A, Picon A, Nuñez M (2018) The microbiota of eight species of dehydrated edible seaweeds from north West Spain. Food Microbiol 70:224–231CrossRefPubMedGoogle Scholar
  40. Dickschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369CrossRefPubMedGoogle Scholar
  41. Dimitrieva GY, Crawford RL, Yuksel GU (2006) The nature of plant growth-promoting effects of a pseudoalteromonad associated with the marine algae Laminaria japonica and linked to catalase excretion. J Appl Microbiol 100:1159–1169CrossRefPubMedGoogle Scholar
  42. Dittami SM, Gravot A, Renault D, Goulitquer S, Eggert A, Bouchereau A, Boyen C, Tonon T (2011) Integrative analysis of metabolite and transcript abundance during the short-term response to saline and oxidative stress in the brown alga Ectocarpus siliculosus. Plant Cell Environ 34:629–642CrossRefPubMedGoogle Scholar
  43. Dittami SM, Duboscq-Bidot L, Perennou M, Gobet A, Corre E, Boyen C, Tonon T (2016) Host–microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME J 10:51–63CrossRefPubMedGoogle Scholar
  44. Dobretsov S, Teplitski M, Paul V (2009) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427CrossRefPubMedGoogle Scholar
  45. Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R, Simon M, Brinkhoff T (2017) Rhodobacteraceae on the marine brown alga Fucus spiralis are abundant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol 40:370–382CrossRefPubMedGoogle Scholar
  46. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890CrossRefPubMedPubMedCentralGoogle Scholar
  47. Dworjanyn SA, Pirozzi I (2008) Induction of settlement in the sea urchin tripneustes gratilla by macroalgae, biofilms and conspecifics: a role for bacteria?. Aquaculture 274:268–274Google Scholar
  48. Egan S, Thomas T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219–225CrossRefPubMedGoogle Scholar
  49. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiol Rev 37:462–476CrossRefPubMedGoogle Scholar
  50. El Shafay SM, Ali SS, El-Sheekh MM (2016) Antimicrobial activity of some seaweeds species from Red Sea, against multidrug resistant bacteria. Egypt J Aquat Res 42:65–74CrossRefGoogle Scholar
  51. El-Shouny WA, Gaafar RM, Ismail GA, Elzanaty MM (2017) Antibacterial activity of some seaweed extracts against multidrug resistant urinary tract bacteria and analysis of their virulence genes. Int J Curr Microbiol Appl Sci 6:2569–2586CrossRefGoogle Scholar
  52. Fernandes N, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2012) Community structure and functional gene profile of bacteria on healthy and diseased thalli of the red seaweed Delisea pulchra. PLoS One 7(12):e50854CrossRefPubMedPubMedCentralGoogle Scholar
  53. Flemming HC, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs)—part I: structural and ecological aspects. Water Sci Tech 43:1–8CrossRefGoogle Scholar
  54. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633CrossRefPubMedPubMedCentralGoogle Scholar
  55. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysia aerophoba. FEMS Microbial Ecol 38:105–113CrossRefGoogle Scholar
  56. Fukui Y, Abe M, Kobayashi M, Yano Y, Satomi M (2014) Isolation of Hyphomonas strains that induce normal morphogenesis in protoplasts of the marine red alga Pyropia yezoensis. Microbiol Ecol 68:556–566CrossRefGoogle Scholar
  57. Gachon C, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15:633–640CrossRefPubMedGoogle Scholar
  58. Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18:1049–1056CrossRefGoogle Scholar
  59. Ghaderiardakani F, Coates JC, Wichard T (2017) Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis (Chlorophyta): a contribution to the lottery theory. FEMS Microbiol Ecol 93:1–12CrossRefGoogle Scholar
  60. Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–300CrossRefGoogle Scholar
  61. Goecke F, Labes A, Wiese J, Schmaljohann R, Imhoff JF (2012) Observation of bacteria over the surface of released oogonia from Fucus vesiculosus L. (Phaeophyceae). Gayana Bot 69:376–379CrossRefGoogle Scholar
  62. Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria—phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24CrossRefGoogle Scholar
  63. Graham L, Wilcox L (1999) Algae. Prentice-Hall, Upper Saddle RiverGoogle Scholar
  64. Graham LE, Knack JJ, Graham ME, Graham JM, Zulkifly S (2015) A metagenome for lacustrine Cladophora (Cladophorales) reveals remarkable diversity of eukaryotic epibionts and genes relevant to materials cycling. J Phycol 51:408–418CrossRefPubMedGoogle Scholar
  65. Greff S, Aires T, Serrão EA, Engelen AH, Thomas OP, Pérez T (2017) The interaction between the proliferating macroalga Asparagopsis taxiformis and the coral Astroides calycularis induces changes in microbiome and metabolomic fingerprints. Sci Rep 7:42625CrossRefPubMedPubMedCentralGoogle Scholar
  66. Grossart HP (2010) Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Environ Microbiol Rep 2:706–714CrossRefPubMedGoogle Scholar
  67. Grueneberg J, Engelen AH, Costa R, Wichard T (2016) Macroalgal morphogenesis induced by waterborne compounds and bacteria in coastal seawater. PLoS One 11:e0146307CrossRefPubMedPubMedCentralGoogle Scholar
  68. Hadfield MG (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu Rev Mar Sci 3:453–470CrossRefGoogle Scholar
  69. Hellio C, Marechal J-P, Veron B, Bremer G, Clare A, Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany coast (France). Mar Biotechnol 6:67–82CrossRefPubMedGoogle Scholar
  70. Hengst MB, Andrade S, González B, Correa JA (2010) Changes in epiphytic bacterial communities of intertidal seaweeds modulated by host, temporality and copper enrichment. Microbiol Ecol 60:282–290CrossRefGoogle Scholar
  71. HMP (2012) The human microbiome project consortium. Structure, function and diversity of the healthy human microbiome. Nature 486:207–214CrossRefGoogle Scholar
  72. Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A (2011a) Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 6:e26458CrossRefPubMedPubMedCentralGoogle Scholar
  73. Hollants J, Decleyre H, Leliaert F, De Clerck O, Willems A (2011b) Life without a cell membrane: challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta). BMC Microbiol 11:e255CrossRefGoogle Scholar
  74. Hollants J, Leliaert F, De Clerck O, Willems A (2013) What we can learn from sushi: a review on seaweed–bacterial associations. FEMS Microbiol Ecol 83:1–16CrossRefPubMedGoogle Scholar
  75. Horincar VB, Parfene G, Tyagi AK, Gottardi D, Dinică R, Guerzoni ME, Bahrim G (2014) Extraction and characterization of volatile compounds and fatty acids from red and green macroalgae from the Romanian Black Sea in order to obtain valuable bioadditives and biopreservatives. J Appl Phycol 26:551–559CrossRefGoogle Scholar
  76. Horta A, Pinteus S, Alves C, Fino N, Silva J, Fernandez S, Rodrigues A, Pedrosa R (2014) Antioxidant and antimicrobial potential of the Bifurcaria bifurcata epiphytic bacteria. Mar Drugs 12:1676–1689CrossRefPubMedPubMedCentralGoogle Scholar
  77. Huggett MJ, Williamson JE, de Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619CrossRefPubMedGoogle Scholar
  78. Ibrahim HAH, Beltagy EA, El-Din NGS, Zokm GME, El-Sikaily AM, Abu-Elela GM (2015) Seaweeds agarophytes and associated epiphytic bacteria along Alexandria coastline, Egypt, with emphasis on the evaluation and extraction of agar and agarose. Rev Biol Mar Oceanogr 50:545–561CrossRefGoogle Scholar
  79. Ismail A, Ktari L, Ahmed M, Bolhuis H, Boudabbous A, Stal LJ, Cretoiu MS, El Bour M (2016) Antimicrobial activities of bacteria associated with the brown alga Padina pavonica. Front Microbiol 7:1072PubMedPubMedCentralGoogle Scholar
  80. JanakiDevi V, YokeshBabu M, Umarani R, Kumaraguru AK (2013) Antagonistic activity of seaweed associated bacteria against human pathogens. Int J Curr Microbiol App Sci 2:140–147Google Scholar
  81. Jha B, Kavita K, Westphal J, Hartmann A, Schmitt-Kopplin P (2013) Quorum sensing inhibition by Asparagopsis taxiformis, a marine macro alga: Separation of the compound that interrupts bacterial communication. Mar Drugs 11:253–265CrossRefPubMedPubMedCentralGoogle Scholar
  82. Joint I, Tait K, Wheeler G (2007) Cross-kingdom signaling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos Trans R Soc Lond B 362:1223–1233CrossRefGoogle Scholar
  83. Jung H, Baek G, Kim J, Shin SG, Lee C (2016) Mild-temperature thermochemical pretreatment of green macroalgal biomass: effects on solubilization, methanation, and microbial community structure. Bioresour Technol 199:326–335CrossRefPubMedGoogle Scholar
  84. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245CrossRefPubMedGoogle Scholar
  85. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140CrossRefPubMedGoogle Scholar
  86. Kanagasabhapathy M, Yamazaki G, Ishida A, Sasaki H, Nagata S (2009) Presence of quorum-sensing inhibitor like compounds from bacteria isolated from the brown alga Colpomenia sinuosa. Lett Appl Microbiol 49:573–579CrossRefPubMedGoogle Scholar
  87. Karthick P, Mohanraju R, Murthy KN, Ramesh CH, Mohandass C, Rajasabapathy R, Kumar SV (2015) Antimicrobial activity of Serratia sp isolated from the coralline red algae Amphiroa anceps. Indian J Geomarine Sci 44:1857–1866Google Scholar
  88. Kavita K, Mishra A, Jha B (2011) Isolation and physico-chemical characterisation of extracellular polymeric substances produced by the marine bacterium Vibrio parahaemolyticus. Biofouling 27:309–317CrossRefPubMedGoogle Scholar
  89. Kientz B, Agogué H, Lavergne C, Marié P, Rosenfeld E (2013) Isolation and distribution of iridescent Cellulophaga and further iridescent marine bacteria in the Charente maritime coast, French Atlantic. coast. Syst Appl Microbiol 36:244–251CrossRefPubMedGoogle Scholar
  90. Kim JY, Park SH, Seo GY, Kim YJ, Oh DC (2015) Winogradskyella eckloniae sp. nov., a marine bacterium isolated from the brown alga Ecklonia cava. Int J Syst Evol Microbiol 65:2791–2796CrossRefPubMedGoogle Scholar
  91. 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 an alginate-degrading bacterial consortium. J Biosci Bioeng 121:286–292CrossRefPubMedGoogle Scholar
  92. KleinJan H, Jeanthon C, Boyen C, Dittami SM (2017) Exploring the cultivable Ectocarpus microbiome. Front Microbiol 8:2456CrossRefPubMedPubMedCentralGoogle Scholar
  93. Kostakioti M, Hadjifrangiskou M, Hultgren SJ (2013) Bacterial biofilms: development, dispersal and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med 3:a010306CrossRefPubMedPubMedCentralGoogle Scholar
  94. Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr Opin Biotechnol 33:125–129CrossRefPubMedGoogle Scholar
  95. Kubanek J, Jensen PR, Keifer PA, Sullards MC, Collins DO, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci 100:6916–6921CrossRefPubMedGoogle Scholar
  96. Kumar V, Zozaya-Valdes E, Kjelleberg S, Thomas T, Egan S (2016) Multiple opportunistic pathogens can cause a bleaching disease in the red seaweed Delisea pulchra. Environ Microbiol 18:3962–3975CrossRefPubMedGoogle Scholar
  97. La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar Drugs 8:988–1010CrossRefPubMedPubMedCentralGoogle Scholar
  98. Lachnit T, Blumel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 5:181–186CrossRefGoogle Scholar
  99. Lachnit T, Wahl M, Harder T (2010) Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26:247–255CrossRefPubMedGoogle Scholar
  100. Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665CrossRefPubMedGoogle Scholar
  101. Lachnit T, Fischer M, Kunzel S, Baines JF, Harder T (2013) Compounds associated with algal surfaces mediate epiphytic colonization of the marine macroalga Fucus vesiculosus. FEMS Microbiol Ecol 84:411–420CrossRefPubMedGoogle Scholar
  102. Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Panse SL, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128–144CrossRefPubMedPubMedCentralGoogle Scholar
  103. Lee JH, Eom SH, Lee EH, Jung YJ, Kim HJ, Jo MR, Son KT, Lee HJ, Kim JH, Lee MS, Kim YM (2014) In vitro antibacterial and synergistic effect of phlorotannins isolated from edible brown seaweed Eisenia bicyclis against acne-related bacteria. Algae 29:47–55Google Scholar
  104. Liu M, Liu Y, Cao MJ, Liu GM, Chen Q, Sun L, Chen H (2017) Antibacterial activity and mechanisms of depolymerized fucoidans isolated from Laminaria japonica. Carbohydr Polym 172:294–305CrossRefPubMedGoogle Scholar
  105. Maheswari MU, Reena A, Sivaraj C (2017) GC-MS analysis, antioxidant and antibacterial activity of the brown algae, Padina tetrastromatica. Int J Pharm Sci Res 8:4014–2400Google Scholar
  106. Mandal SK, Singh RP, Patel V (2011) Isolation and characterization of exopolysaccharide secreted by a toxic dinoflagellate, Amphidinium carterae Hulburt 1957 and its probable role in harmful algal blooms (HABs). Microb Ecol 62:518–527CrossRefPubMedGoogle Scholar
  107. Manilal A, Sujith S, Sabarathnam B, Kiran G, Selvin J, Shakir C, Lipton AP (2010) Bioactivity of the red alga Asparagopsis taxiformis collected from the south-western coast of India. Braz J Oceonogr 58:93–100CrossRefGoogle Scholar
  108. Manivannan K, Karthikai devi G, Anantharaman P, Balasubramanian T (2011) Antimicrobial potential of selected brown seaweeds from Vedalai coastal waters, Gulf of Mannar. Asian Pac J Trop Biomed 1:114–120CrossRefPubMedPubMedCentralGoogle Scholar
  109. Marshall K, Joint I, Callow ME, Callow JA (2006) Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza. Microb Ecol 52:302–310CrossRefPubMedGoogle Scholar
  110. Martin M, Portetelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae, diversity, interactions and biotechnological applications. Appl Microbiol Biot 98:2917–2935CrossRefGoogle Scholar
  111. 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 6:1487CrossRefPubMedPubMedCentralGoogle Scholar
  112. Menaa F (2015) Tapping into deep-water reservoirs to overcome antibiotic resistance through bacteria-producing unique secondary metabolites. Pharmaceut Analyt Acta 6:e172Google Scholar
  113. Meena VD, Dotaniya ML, Saha JK, Patra AK (2015) Antibiotics and antibiotic resistant bacteria in wastewater: impact on environment, soil microbial activity and human health. Afr J Microbiol Res 9:965–978Google Scholar
  114. Mesquita MMF, Baddini ALQ, Netto ADP, Araujo JM, Salgueiro F, Filho EAPL, De-Paula JC, Fleury BG, Cavalcanti DN, Teixeira VL (2015) Chemical similarity between Dictyota caribaea and Dictyota menstrualis (Dictyotaceae, Phaeophyceae) from the coast of Rio de Janeiro, Brazil. Biochem Syst Ecol 58:97–101CrossRefGoogle Scholar
  115. Miranda LN, Hutchison K, Grossman AR, Brawley SH (2013) Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS One 8:e58269CrossRefPubMedPubMedCentralGoogle Scholar
  116. Moon HE, Islam N, Ahn BR, Chowdhury SS, Sohn HS, Jung HA, Choi JS (2011) Protein tyrosine phosphatase 1B and α-glucosidase inhibitory phlorotannins from edible brown algae, Ecklonia stolonifera and Eisenia bicyclis. Biosci Biotechnol Biochem 75:1472–1480CrossRefPubMedGoogle Scholar
  117. Moorthi PV, Balasubramanian C (2015) Antimicrobial properties of marine seaweed, Sargassum muticum against human pathogens. J Coast Life Med 3:122–125Google Scholar
  118. Murray PM, Moane S, Collins C, Beletskaya T, Thomas OP, Duarte AW, Nobre FS, Owoyemi IO, Pagnocca FC, Sette LD, McHugh E, Causse E, Pérez-López P, Feijoo G, Moreira MT, Rubiolo J, Leirós M, Botana LM, Pinteus S, Alves C, Horta A, Pedrosa R, Jeffryes C, Agathos SN, Allewaert C, Verween A, Vyverman W, Laptev I, Sineoky S, Bisio A, Manconi R, Ledda F, Marchi M, Pronzato R, Walsh DJ (2013) Sustainable production of biologically active molecules of marine based origin. New Biotechnol 30:839–850CrossRefGoogle Scholar
  119. Murugan A, Begum MS, Ramasamy MS, Raja P (2012) Antifouling and antipredatory activity of natural products of the seaweeds Dictyota dichotoma and Chaetomorpha linoides. Nat Prod Res 26:975–978CrossRefPubMedGoogle Scholar
  120. Nylund GM, Persson F, Lindegarth M, Cervin G, Hermansson M, Pavia H (2010) The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol Ecol 71:84–93CrossRefPubMedGoogle Scholar
  121. Nylund GM, Enge S, Pavia H (2013) Costs and benefits of chemical defense in the red alga Bonnemaisonia hamifera. PLoS One 8(4):e61291CrossRefPubMedPubMedCentralGoogle Scholar
  122. Ojha AK, Verma A, Pal Y, Bhatt D, Mayilraj S, Krishnamurthi S (2017) Marinomonas epiphytica sp. nov., isolated from a marine intertidal macroalga. Int J Syst Evol Microbiol 67:2746–2751CrossRefPubMedGoogle Scholar
  123. Othmani A, Bunet R, Bonnefont JL, Briand JF, Culioli G (2016) Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria. J Appl Phycol 28:1975–1986CrossRefGoogle Scholar
  124. Pedersén M, (1968) Ectocarpus fasciculatus: Marine brown alga requiring kinetin. Nature 218 (5143):776–776Google Scholar
  125. Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S (2009) Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol 69:113–124CrossRefPubMedGoogle Scholar
  126. Penesyan A, Kjelleberg S, Egan S (2010) Development of novel drugs from marine surface associated microorganisms. Mar Drugs 8:438–459CrossRefPubMedPubMedCentralGoogle Scholar
  127. Penesyan A, Gillings M, Paulsen IT (2015) Antibiotic discovery: combatting bacterial resistance in cells and in biofilm communities. Molecules 20:5286–5298CrossRefPubMedPubMedCentralGoogle Scholar
  128. Penesyan A, Tebben J, Lee M, Thomas T, Kjelleberg S, Harder T, Egan S (2011) Identification of the antibacterial compound produced by the marine epiphytic bacterium pseudovibrio sp. D323 and related sponge-associated bacteria. Mar Drugs 9(8):1391–1402Google Scholar
  129. Peters A, Marie D, Scornet D, Kloareg B, Cock J (2004) Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetic sand genomics. J Phycol 40:1079–1088CrossRefGoogle Scholar
  130. Potin P (2008) Oxidative burst and related responses in biotic interactions of algae. In: Amsler CH (ed) Algal chemical ecology. Springer, Berlin, pp 245–271CrossRefGoogle Scholar
  131. Prasad K, Das AK, Oza MD, Brahmbhatt H, Siddhanta AK, Meena R, Eswaran K, Rajyaguru MR, Ghosh PK (2010) Detection and quantification of some plant growth regulators in a seaweed-based foliar spray employing a mass spectrometric technique sans chromatographic separation. J Agric Food Chem 58:4594–4601CrossRefPubMedGoogle Scholar
  132. Provasoli L, Carlucci AF (1974) Vitamins and growth regulators. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell, Oxford, pp 74–87Google Scholar
  133. Rahelivao MP, Gruner M, Andriamanantoanina H, Bauer I, Knolker HJ (2015) Brown algae (Phaeophyceae) from the coast of Madagascar: preliminary bioactivity studies and isolation of natural products. Nat Prod Bioprospect 5:223–235CrossRefPubMedPubMedCentralGoogle Scholar
  134. Rajivgandhi G, Vijayan R, Kannan M, Santhanakrishnan M, Manoharan N (2016) Molecular characterization and antibacterial effect of endophytic actinomycetes Nocardiopsis sp. GRG1 (KT235640) from brown algae against MDR strains of uropathogens. Bioactive Materials 1:140–150CrossRefPubMedPubMedCentralGoogle Scholar
  135. Rao D, Webb JS, Holmström C, Case R, Low A, Steinberg P, Kjelleberg S (2007) Low densities of epiphytic bacteria from the marine alga Ulva australis inhibit settlement of fouling organisms. Appl Environ Microbiol 73:7844–7852CrossRefPubMedPubMedCentralGoogle Scholar
  136. Ravisankar A, Gnanambal ME, Sundaram LR (2013) A newly isolated Pseudomonas sp., epibiotic on the seaweed, Padina tetrastromatica, off southeastern coast of India, reveals antibacterial action. Appl Biochem Biotechnol 171:1968–1985CrossRefPubMedGoogle Scholar
  137. Rizzo L, Pusceddu A, Stabili L, Alifano P, Fraschetti S (2017) Potential effects of an invasive seaweed (Caulerpa cylindracea, Sonder) on sedimentary organic matter and microbial metabolic activities. Sci Rep 7:12113.  https://doi.org/10.1038/s41598-017-12556-4 CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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 cultivatable marine bacteria and to investigate their adaptive metabolism. Talanta 80:1758–1770CrossRefPubMedGoogle Scholar
  139. Satheesh S, Ba-akdah MA, Al-Sofyani AA (2016) Natural antifouling compound production by microbes associated with marine macroorganisms—a review. Electron J Biotechnol 21:26–35CrossRefGoogle Scholar
  140. Schmidt TSB, Rodrigues JFM, von Mering C (2014) Ecological consistency of SSU rRNA-based operational taxonomic units at a global scale. PLoS Comput Biol 10(4):e1003594CrossRefPubMedPubMedCentralGoogle Scholar
  141. Schwartz N, Rohde S, Dobretsov S, Hiromori S, Schupp PJ (2017) The role of chemical antifouling defence in the invasion success of Sargassum muticum: a comparison of native and invasive brown algae. PLoS One 12(12):e0189761CrossRefPubMedPubMedCentralGoogle Scholar
  142. Silva FS, Bitencourt JAP, Savergnini F, Guerra LV, Baptista-Neto JA, Crapez MAC (2011) Bioavailability of organic matter in the superficial sediment of Guanabara Bay, Rio de Janeiro, Brazil. Anuario do Instituto de Geociencias 34:52–63Google Scholar
  143. Singh RP, Reddy CRK (2014) Seaweed–microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230CrossRefPubMedGoogle Scholar
  144. Singh RP, Mantri VA, Reddy CRK, Jha B (2011a) Isolation of seaweed-associated bacteria and their morphogenesis inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol 12:13–21CrossRefGoogle Scholar
  145. Singh RP, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2011b) Role of bacterial isolates in enhancing the bud induction in the industrially important red alga Gracilaria dura. FEMS Microbiol Ecol 76:381–392CrossRefPubMedGoogle Scholar
  146. Singh RP, Shukla MK, Mishra A, Kumari P, Reddy CRK, Jha B (2011c) Isolation and characterization of exopolysaccharides from seaweed-associated bacteria Bacillus licheniformis. Carbohydr Polym 84:1019–1026CrossRefGoogle Scholar
  147. Singh RP, Shukla MK, Mishra A, Reddy CRK, Jha B (2013) Bacterial extracellular polymeric substances and their effect on settlement of zoospore of Ulva fasciata. Colloids Surf B 103:223–230CrossRefGoogle Scholar
  148. Singh RP, Baghel RS, Reddy CRK, Jha B (2015) Effect of quorum sensing signals produced by seaweed-associated bacteria on carpospores liberation from Gracilaria dura. Front Plant Sci 6:117PubMedPubMedCentralGoogle Scholar
  149. Sousa C, Gangadhar KN, Morais TR, Conserva GA, Vizetto-Duarte C, Pereira H, Laurenti MD, Campino L, Levy D, Uemi M, Barreira L, Custódio L, Passero LF, Lago JH, Varela J (2017) Antileishmanial activity of meroditerpenoids from the macroalgae Cystoseira baccata. Exp Parasitol 174:1-9Google Scholar
  150. Sneed JM, Pohnert G (2010) The green macroalga Dictyosphaeria ocellata influences the structure of the bacterioplankton community through differential effects on individual bacterial phylotypes. FEMS Microbiol Ecol 75:242–254CrossRefPubMedGoogle Scholar
  151. Sneed JM, Pohnert G (2011) The green alga Dicytosphaeria ocellata and its organic extracts alter natural bacterial biofilm communities. Biofouling 27:347–356CrossRefPubMedGoogle Scholar
  152. Soares AR, da Gama BAP, da Cunha AP, Teixeira VL, Pereira RC (2008) Induction of attachment of the mussel Perna perna by natural products from the brown seaweed Stypopodium zonale. Mar Biotechnol 10:158–165CrossRefPubMedGoogle Scholar
  153. Spavieri J, Allmendinger A, Kaiser M, Casey R, Hingley-Wilson S, Lalvani A, Guiry MD, Blunden G, Tasdemir D (2010) Antimycobacterial, antiprotozoal and cytotoxic potential of twenty-one brown algae (Phaeophyceae) from British and Irish waters. Phytother Res 24:1724–1729CrossRefPubMedGoogle Scholar
  154. Spilling K, Titelman J, Greve TM, Kühl M (2010) Microsensor measurements of the external and internal microenvironment of Fucus vesiculosus (Phaeophyceae). J Phycol 46:1350–1355CrossRefGoogle Scholar
  155. Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertel W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48:1433–1447CrossRefPubMedGoogle Scholar
  156. Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77CrossRefPubMedGoogle Scholar
  157. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  158. Steinberg PD, de Nys R, Kjelleberg S (1998) Chemical inhibition of epibiota by Australian seaweeds. Biofouling 12:227–244CrossRefGoogle Scholar
  159. Steinberg PD, de Nys R, Kjelleberg S (2002) Chemical cues for surface colonization. J Chem Ecol 28:1935–1951CrossRefPubMedGoogle Scholar
  160. Suresh M, Iyapparaj P, Anantharaman P (2016) Antifouling activity of lipidic metabolites derived from Padina tetrastromatica. Appl Biochem Biotechnol 179:805–818CrossRefPubMedGoogle Scholar
  161. Susilowati R, Sabdono A, Widowati I (2015) Isolation and characterization of bacteria associated with brown algae Sargassum spp. from Panjang Island and their antibacterial activities. Procedia Environ Sci 23:240–246CrossRefGoogle Scholar
  162. Tapia JE, González B, Goulitquer S, Potin P, Correa JA (2016) Microbiota influences morphology and reproduction of the brown alga Ectocarpus sp. Front Microbiol 7:197CrossRefPubMedPubMedCentralGoogle Scholar
  163. Teixeira VL (2013) Produtos naturais de algas marinhas bentônicas. Rev Virtual Quim 5:343–362CrossRefGoogle Scholar
  164. Thennarasan S, Murugesan S (2015) Antibacterial activity of crude methanolic extract of marine brown alga Lobophora variegata (J.V. Lamouroux). World J Pharm Res 4:1714–1722Google Scholar
  165. Torralba MG, Franks JS, Gomez A, Yooseph S, Nelson KE, Grimes DJ (2017) Effect of Macondo Prospect 252 oil on microbiota associated with pelagic Sargassum in the northern Gulf of Mexico. Microb Ecol 73:91–100CrossRefPubMedGoogle Scholar
  166. Trias R, García-Lledó A, Sánchez N, López-Jurado JL, Hallin S, Bañeras L (2012) Abundance and composition of epiphytic bacterial and archaeal ammonia oxidizers of marine red and brown macroalgae. Appl Environ Microbiol 78:318–325CrossRefPubMedPubMedCentralGoogle Scholar
  167. Tujula NA, Holmström C, Mußmann M, Amann R, Kjelleberg S, Crocetti GR (2006) A CARD-FISH protocol for the identification and enumeration of epiphytic bacteria on marine algae. J Microbiol Methods 65:604–607CrossRefPubMedGoogle Scholar
  168. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmström C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine ulvacean alga. ISME J 4:301–311CrossRefPubMedGoogle Scholar
  169. Twigg MS, Tait K, Williams P, Atkinson S, Cámara M (2013) Interference with the germination and growth of Ulva zoospores by quorum-sensing molecules from Ulva-associated epiphytic bacteria. Environ Microbiol 16:445–453CrossRefPubMedPubMedCentralGoogle Scholar
  170. Uzair B, Menaa F, Khan BA, Mohammad FV, Ahmad VU, Djeribi R, Menaa B (2018) Isolation, purification, structural elucidation and antimicrobial activities of Kocumarin, a novel antibiotic isolated from actinobacterium Kocuria marina CMG S2 associated with the brown seaweed Pelvetia canaliculata. Microbiol Res 206:186–197CrossRefPubMedGoogle Scholar
  171. Vaikundamoorthy R, Krishnamoorthy V, Vilwanathan R, Rajendran R (2018) Structural characterization and anticancer activity (MCF7 and MDA-MB-231) of polysaccharides fractionated from brown seaweed Sargassum wightii. Int J Biol Macromol 111:1229–1237CrossRefPubMedGoogle Scholar
  172. Vairappan CS, Suzuki M, Motomura T, Ichimura T (2001) Pathogenic bacteria associated with lesions and thallus bleaching symptoms in the Japanese kelp Laminaria religiosa Miyabe (Laminariales, Phaeophyceae). Hydrobiologia 445:183–191CrossRefGoogle Scholar
  173. Vairappan CS, Chung CS, Hurtado AQ, Soya FE, Lhonneur GB, Critchley A (2008) Distribution and symptoms of epiphyte infection in major carrageenophyte-producing farms. J Appl Phycol 20:477–483CrossRefGoogle Scholar
  174. Vairappan CS, Anangdan SP, Tan KL, Matsunaga S (2010) Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. J Appl Phycol 22:305–311CrossRefGoogle Scholar
  175. Vesty EF, Kessler RW, Wichard T, Coates JC (2015) Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture. Front Plant Sci 6:1–8CrossRefGoogle Scholar
  176. Vieira C, Engelen AH, Guentas L, Aires T, Houlbreque F, Gaubert J, Serrão EA, De Clerck O, Payri CE (2016) Species specificity of bacteria associated to the brown seaweeds Lobophora (Dictyotales, Phaeophyceae) and their potential for induction of rapid coral bleaching in Acropora muricata. Front Microbiol 7:316Google Scholar
  177. Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F (2012) The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol 3:292CrossRefPubMedPubMedCentralGoogle Scholar
  178. Wang G, Shuai L, Li Y, Lin W, Zhao X, Duan D (2008) Phylogenetic analysis of epiphytic marine bacteria on hole-rotten diseased sporophytes of Laminaria japonica. J Appl Phycol 20:403–409CrossRefGoogle Scholar
  179. Weinberger F, Beltran J, Correa JA, Pohnert G, Kumar N, Steinberg P, Kloareg B, Potin P (2007) Spore release in Acrochaetium sp. (Rhodophyta) is bacterially controlled. J Phycol 43:235–241CrossRefGoogle Scholar
  180. Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 6:86Google Scholar
  181. Wiese J, Thiel V, Nagel K, Staufenberger T, Imhoff JF (2009) Diversity of antibiotic active bacteria associated with the brown alga Laminaria saccharina from the Baltic Sea. Mar Biotechnol 11:287–300CrossRefPubMedGoogle Scholar
  182. Yagi H, Fujise A, Itabashi N, Ohshiro T (2016) Purification and characterization of a novel alginate lyase from the marine bacterium Cobetia sp. NAP1 isolated from brown algae. Biosci Biotechnol Biochem 80:2338–2346CrossRefPubMedGoogle Scholar
  183. Zozaya-Valdes E, Egan S, Thomas T (2015) A comprehensive analysis of the microbial communities of healthy and diseased marine macroalgae and the detection of known and potential bacterial pathogens. Front Microbiol 6:146Google Scholar
  184. Zozaya-Valdes E, Roth-Schulze AJ, Egan S, Thomas T (2017) Microbial community function in the bleaching disease of the marine macroalgae Delisea pulchra. Environ Microbiol 19:3012–3024CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Michelle Marchezan F. de Mesquita
    • 1
    Email author
  • Mirian A. C. Crapez
    • 1
  • Valéria L. Teixeira
    • 2
    • 3
  • Diana N. Cavalcanti
    • 1
  1. 1.Postgraduate Program in Marine Biology and Coastal Environments, Department of Marine Biology, Institute of BiologyFluminense Federal UniversityNiteróiBrazil
  2. 2.Postgraduate Program in Science and Biotechnology, Institute of BiologyFluminense Federal UniversityNiteróiBrazil
  3. 3.Postgraduate Program in Neotropical Biodiversity, from the Institute of BiosciencesFederal University of Rio de Janeiro (UNIRIO)Rio de JaneiroBrazil

Personalised recommendations