Advertisement

Bacterial Communities on Macroalgae

  • Michael W. Friedrich
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 219)

Abstract

Microorganisms play an important role in the biology of macroalgae. A number of important functions, ranging from growth enhancement, production of toxins and other secondary metabolites, regulation of morphology, and settlement of invertebrate larvae and spores to pathogenicity, have been ascribed to microorganisms, mostly based on cultivation approaches. Yet, the composition, structuring, and dynamics of microorganisms present on the algal host have been scarcely studied so far using cultivation-independent molecular methods. This chapter focuses on recent insights into the composition of the bacterial microbiota associated with macroalgae gained by gene sequence-based analysis.

Keywords

Microbial Community Coral Reef Clone Library Terminal Restriction Fragment Length Polymorphism Lateral Gene Transfer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

I would like to thank Kai Bischof for the possibility to gain insights into the field of algae–microbe communities and helpful suggestions on algal taxonomy. Manuscript preparation was supported by the University of Bremen.

References

  1. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedCentralPubMedGoogle Scholar
  2. Armstrong E, Rogerson A, Leftley JW (2000) The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar Coast Shelf Sci 50:415–424CrossRefGoogle Scholar
  3. 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 13:1192–1204PubMedCrossRefGoogle Scholar
  4. Bengtsson MM, Ovreas L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bengtsson MM, Sjotun K, Ovreas L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83CrossRefGoogle Scholar
  6. Bengtsson MM, Sjotun K, Storesund JE, Ovreas L (2011) Utilization of kelp-derived carbon sources by kelp surface-associated bacteria. Aquat Microb Ecol 62:191–199CrossRefGoogle Scholar
  7. Bolinches J, Lemos ML, Barja JL (1988) Population dynamics of heterotrophic bacterial vommunities associated with Fucus vesiculosus and Ulva rigida in an estuary. Microb Ecol 15:345–357PubMedCrossRefGoogle Scholar
  8. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108:14288–14293PubMedCentralPubMedCrossRefGoogle Scholar
  9. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011b) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600PubMedCentralPubMedCrossRefGoogle Scholar
  10. Chan ECS, Mcmanus EA (1969) Distribution characterization and nutrition of marine microorganisms from algae Polysiphonia Lanosa and Ascophyllum Nodosum. Can J Microbiol 15:409–420PubMedCrossRefGoogle Scholar
  11. Correa JA (1997) Infectious diseases of marine algae: current knowledge and approaches. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress, Bristol, UK, pp 149–180Google Scholar
  12. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93PubMedCrossRefGoogle Scholar
  13. Croft MT, Warren MJ, Smith AG (2006) Algae need their vitamins. Eukaryot Cell 5:1175–1183PubMedCentralPubMedCrossRefGoogle Scholar
  14. Dobretsov SV, Qian PY (2002) Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18:217–228CrossRefGoogle Scholar
  15. Egan S, Thomas T, Holmstrom C, Kjelleberg S (2000) Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environ Microbiol 2:343–347PubMedCrossRefGoogle Scholar
  16. Egan S, Holmstrom C, Kjelleberg S (2001) Pseudoalteromonas ulvae sp nov., a bacterium with antifouling activities isolated from the surface of a marine alga. Int J Syst Evol Microbiol 51:1499–1504PubMedGoogle Scholar
  17. Egan S, Thomas T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219–225PubMedCrossRefGoogle Scholar
  18. Eilers H, Pernthaler J, Gloeckner FO, Amann R (2000) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66:3044–3051PubMedCentralPubMedCrossRefGoogle Scholar
  19. Fuhrman JA, Campbell L (1998) Microbial microdiversity. Nature 393:410–411CrossRefGoogle Scholar
  20. Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–299CrossRefGoogle Scholar
  21. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507PubMedCrossRefGoogle Scholar
  22. Hengst MB, Andrade S, Gonzalez B, Correa JA (2010) Changes in epiphytic bacterial communities of intertidal seaweeds modulated by host, temporality, and copper enrichment. Microb Ecol 60:282–290PubMedCrossRefGoogle Scholar
  23. Huggett MJ, Crocetti GR, Kjelleberg S, Steinberg PD (2008) Recruitment of the sea urchin Heliocidaris erythrogramma and the distribution and abundance of inducing bacteria in the field. Aquat Microb Ecol 53:161–171CrossRefGoogle Scholar
  24. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406PubMedCentralPubMedCrossRefGoogle Scholar
  25. Jensen PR, Kauffman CA, Fenical W (1996) High recovery of culturable bacteria from the surfaces of marine algae. Mar Biol 126:1–7CrossRefGoogle Scholar
  26. Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P, Camara M (2002) Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 298:1207PubMedCrossRefGoogle Scholar
  27. Joint I, Tait K, Wheeler G (2007) Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos Trans R Soc Lond B Biol Sci 362:1223–1233PubMedCentralPubMedCrossRefGoogle Scholar
  28. Keshtacherliebson E, Hadar Y, Chen Y (1995) Oligotrophic bacteria enhance algal growth under iron-deficient conditions. Appl Environ Microbiol 61:2439–2441Google Scholar
  29. 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 13:655–665PubMedCrossRefGoogle Scholar
  30. Largo DB, Fukami K, Nishijima T (1995) Occasional pathogenic bacteria promoting ice-ice disease in the carrageenan producing red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 7:545–554CrossRefGoogle Scholar
  31. Largo DB, Fukami K, Adachi M, Nishijima T (1997) Direct enumeration of bacteria from macroalgae by epifluorescence microscopy as applied to the fleshy red algae Kappaphycus alvarezii and Gracilaria spp. (Rhodophyta). J Phycol 33:554–557CrossRefGoogle Scholar
  32. Largo DB, Fukami K, Nishijima T (1999) Time-dependent attachment mechanism of bacterial pathogen during ice-ice infection in Kappaphycus alvarezii (Gigartinales, Rhodophyta). J Appl Phycol 11:129–136CrossRefGoogle Scholar
  33. Lewis TE, Garland CD, Mcmeekin TA (1985) The bacterial biota on crustose (nonarticulated) coralline algae from tasmanian waters. Microb Ecol 11:221–230PubMedCrossRefGoogle Scholar
  34. Liesack W, Janssen PH, Rainey FA, Ward-Rainey NL, Stackebrandt E (1997) Microbial diversity in soil: the need for a combined approach using molecular and cultivation techniques. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker, New York, pp 375–439Google Scholar
  35. Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522PubMedCentralPubMedGoogle Scholar
  36. Liu M, Dong Y, Zhao Y, Zhang GT, Zhang WC, Xiao T (2011) Structures of bacterial communities on the surface of Ulva prolifera and in seawaters in an Ulva blooming region in Jiaozhou Bay, China. World J Microbiol Biotechnol 27:1703–1712CrossRefGoogle Scholar
  37. Longford SR, Tujula NA, Crocetti GR, Holmes AJ, Holmstrom C, Kjelleberg S et al (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229CrossRefGoogle Scholar
  38. Marsh TL (2005) Culture-independent microbial community analysis with terminal restriction fragment length polymorphism. Environ Microbiol 397:308–329Google Scholar
  39. 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 52:302–310PubMedCrossRefGoogle Scholar
  40. 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 5:25–35PubMedCrossRefGoogle Scholar
  41. Meusnier I, Olsen JL, Stam WT, Destombe C, Valero M (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 10:931–946PubMedCrossRefGoogle Scholar
  42. Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedCentralPubMedGoogle Scholar
  43. Nakanishi K, Nishijima M, Nishimura M, Kuwano K, Saga N (1996) Bacteria that induce morphogenesis in Ulva pertusa (chlorophyta) grown under axenic conditions. J Phycol 32:479–482CrossRefGoogle Scholar
  44. Namba A, Shigenobu Y, Kobayashi M, Kobayashi T, Oohara I (2010) A new primer for 16S rDNA analysis of microbial communities associated with Porphyra yezoensis. Fisheries Sci 76:873–878CrossRefGoogle Scholar
  45. Ohkubo S, Miyashita H, Murakami A, Takeyama H, Tsuchiya T, Mimuro M (2006) Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. Appl Environ Microbiol 72:7912–7915PubMedCentralPubMedCrossRefGoogle Scholar
  46. Olson JB, Kellogg CA (2010) Microbial ecology of corals, sponges, and algae in mesophotic coral environments. FEMS Microbiol Ecol 73:17–30PubMedCrossRefGoogle Scholar
  47. Pace NR, Stahl DA, Lane DJ, Olsen GJ (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv Microb Ecol 9:1–55CrossRefGoogle Scholar
  48. Patel P, Callow ME, Joint I, Callow JA (2003) Specificity in the settlement–modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha. Environ Microbiol 5:338–349PubMedCrossRefGoogle Scholar
  49. Pernthaler J, Amann R (2005) Fate of heterotrophic microbes in pelagic habitats: focus on populations. Microbiol Mol Biol Rev 69:440–461PubMedCentralPubMedCrossRefGoogle Scholar
  50. Provasoli L, Pintner IJ (1980) Bacteria induced polymorphism in an axenic laboratory strain of Ulva lactuca (Chlorophyceae). J Phycol 16:196–201CrossRefGoogle Scholar
  51. Raghukumar C, Nagarkar S, Raghukumar S (1992) Association of thraustochytrids and fungi with living marine algae. Mycol Res 96:542–546CrossRefGoogle Scholar
  52. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394PubMedCrossRefGoogle Scholar
  53. Rossello-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedCrossRefGoogle Scholar
  54. Sale PF (1979) Recruitment, loss and coexistence in a guild of territorial coral-reef fishes. Oecologia 42:159–177CrossRefGoogle Scholar
  55. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120PubMedCentralPubMedCrossRefGoogle Scholar
  56. Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77PubMedCrossRefGoogle Scholar
  57. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  58. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmstrom C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 4:301–311PubMedCrossRefGoogle Scholar
  59. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–4U7PubMedCentralPubMedCrossRefGoogle Scholar
  60. 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
  61. Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438PubMedCrossRefGoogle Scholar
  62. Wang G, Shuai L, Li Y, Lin W, Zhao XW, Duan DL (2008) Phylogenetic analysis of epiphytic marine bacteria on Hole-Rotten diseased sporophytes of Laminaria japonica. J Appl Phycol 20:403–409CrossRefGoogle Scholar
  63. Weinberger F, Friedlander M, Gunkel W (1994) A bacterial facultative parasite of Gracilaria-Conferta. Dis Aquat Organ 18:135–141CrossRefGoogle Scholar
  64. Weinberger F, Beltran J, Correa JA, Lion U, Pohnert G, Kumar N et al (2007) Spore release in Acrochaetium sp (Rhodophyta) is bacterially controlled. J Phycol 43:235–241CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.BreMarE - Bremen Marine Ecology, Faculty of Biology/ChemistryUniversity of BremenBremenGermany

Personalised recommendations