Abstract
Kelp forests worldwide are known as hotspots for macroscopic biodiversity and primary production, yet very little is known about the biodiversity and roles of microorganisms in these ecosystems. Secondary production by heterotrophic bacteria associated to kelp is important in the food web as a link between kelp primary production and kelp forest consumers. The aim of this study was to investigate the relationship between bacterial diversity and two important processes in this ecosystem; bacterial secondary production and primary succession on kelp surfaces. To address this, kelp, Laminaria hyperborea, from southwestern Norway was sampled at different geographical locations and during an annual cycle. Pyrosequencing (454-sequencing) of amplicons of the 16S rRNA gene of bacteria was used to study bacterial diversity. Incorporation of tritiated thymidine was used as a measure of bacterial production. Our data show that bacterial diversity (richness and evenness) increases with the age of the kelp surface, which corresponds to the primary succession of its bacterial communities. Higher evenness of bacterial operational taxonomical units (OTUs) is linked to higher bacterial production. Owing to the dominance of a few abundant OTUs, kelp surface biofilm communities may be characterized as low-diversity habitats. This is the first detailed study of kelp-associated bacterial communities using high-throughput sequencing and it extends current knowledge on microbial community assembly and dynamics on living surfaces.
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Abdullah M, Fredriksen S . (2004). Production, respiration and exudation of dissolved organic matter by the kelp Laminaria hyperborea along the west coast of Norway. J Mar Biol Assoc UK 84: 887–894.
Bengtsson MM, Øvreås L . (2010). Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. Bmc Microbiol 10: 261.
Bengtsson MM, Sjøtun K, Øvreås L . (2010). Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60: 71–83.
Bengtsson MM, Sjøtun K, Storesund JE, Øvreås L . (2011). Utilization of kelp-derived carbon sources by kelp surface-associated bacteria. Aquat Microb Ecol 62: 191–199.
Bernardino AF, Smith CR, Baco A, Altamira I, Sumida PYG . (2010). Macrofaunal succession in sediments around kelp and wood falls in the deep NE Pacific and community overlap with other reducing habitats. Deep-Sea Res Part I 57: 708–723.
Bradley RA, Bradley DW . (1993). Wintering shorebirds increase after kelp (Macrocystis) recovery. Condor 95: 372–376.
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 108: 14288–14293.
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: 590–600.
Chao A . (1987). Estimating the population-size for capture recapture data with unequal catchability. Biometrics 43: 783–791.
Christie H, Jorgensen N, Norderhaug K, Waage-Nielsen E . (2003). Species distribution and habitat exploitation of fauna associated with kelp (Laminaria hyperborea) along the Norwegian coast. J Mar Biol Assoc UK 83: 687–699.
Coyer JA . (1984). The invertebrate assemblage associated with the giant kelp, Macrocystis pyrifera, at Santa Catalina island, California: A general description with emphasis on amphipods, copepods, mysids, and shrimps. Fish B-Noaa 82: 55–66.
Duggins D, Simenstad CA, Estes JA . (1989). Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245: 170–173.
Dunton KH, Reimnitz E, Schonberg S . (1982). An arctic kelp community in the Alaskan Beaufort Sea. Arctic 35: 465–484.
Evans LV, Simpson M, Callow ME . (1973). Sulphated polysaccharide synthesis in brown algae. Planta 110: 237–252.
Fierer N, Nemergut D, Knight R, Craine JM . (2010). Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161: 635–642.
Fredriksen S . (2003). Food web studies in a Norwegian kelp forest based on stable isotope (delta C-13 and delta N-15) analysis. Mar Ecol Prog Ser 260: 71–81.
Fuhrman JA, Azam F . (1980). Bacterioplankton secondary production estimates for coastal waters of British-Columbia, Antarctica, and California. Appl Environ Microb 39: 1085–1095.
Fuhrman JA, Azam F . (1982). Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar Biol 66: 109–120.
Graham MH, Kinlan BP, Druehl LD, Garske LE, Banks S . (2007). Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc Natl Acad Sci USA 104: 16576–16580.
Harrold C, Light K, Lisin S . (1998). Organic enrichment of submarine-canyon and continental-shelf benthic communities by macroalgal drift imported from nearshore kelp forests. Limnol Oceanogr 43: 669–678.
Hooper D, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S et al. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75: 3–35.
Hubbell SP . (2005). Neutral theory in community ecology and the hypothesis of functional equivalence. Funct Ecol 19: 166–172.
Hubbell SP . (2001). The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press: Princeton, NJ, USA, p 375.
Isaeus M . (2004). Factors structuring Fucus communities at open and complex coastlines in the Baltic Sea. Doctoral Thesis, University of Stockholm, Sweden.
Jeffrey WH, Paul JH . (1990). Thymidine uptake, thymidine incorporation, and thymidine kinase-activity in marine bacterium isolates. Appl Environ Microb 56: 1367–1372.
Kain JM . (1971). Synopsis of biological data on Laminaria hyperborea. FAO Fisheries Synopsis 87.
Kain JM . (1979). A view of the genus Laminaria. Oceanogr Mar Biol Ann Rev 17: 101–161.
Koop K, Carter RA, Newell RC . (1982). Mannitol-fermenting bacteria as evidence for export from kelp beds. Limnol Oceanogr 27: 950–954.
Küpper FC, Müller DG, Peters A, Kloareg B, Potin P . (2002). Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of laminariales. J Chem Ecol 28: 2057–2081.
Lachnit T, Meske D, Wahl M, Harder T, Schmitz R . (2010). Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13: 655–665.
Langenheder S, Bulling MT, Solan M, Prosser JI . (2010). Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLoS One 5: e10834.
Lee K, Lee HK, Choi T-H, Kim K-MT, Cho J-C . (2007). Granulosicoccaceae fam. nov., to include Granulosicoccus antarcticus gen. nov., sp. nov., a non-phototrophic, obligately aerobic chemoheterotroph in the order Chromatiales, isolated from antarctic Seawater. J Microbiol Biotechnol 17: 1483–1490.
Legendre P, Gallagher E . (2001). Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.
Longford R, Tujula NA, Crocetti GR, Holmes AJ, Holmstroem C, Kjelleberg S . (2007). Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48: 217–229.
Mann KH . (1973). Seaweeds - their productivity and strategy for growth. Science 182: 975–981.
Naeem S, Hahn D, Schuurman G . (2000). Producer-decomposer co-dependency influences biodiversity effects. Nature 403: 762–764.
Newell RC, Field JG . (1983). The contribution of bacteria and detritus to carbon and nitrogen flow in a benthic community. Mar Biol Lett 4: 23–36.
Newell RC, Lucas MI . (1981). The quantitative significance of dissolved and particulate organic matter released during fragmentation of kelp in coastal waters. Kieler Meeresforch Sonderh 5: 356–369.
Newell RC, Lucas MI, Velimirov B, Seiderer LJ . (1980). Quantitative significance of dissolved organic losses following fragmentation of Kelp (Ecklonia maxima and Laminaria pallida). Mar Ecol Prog Ser 2: 45–59.
Norderhaug KM, Christie H, Fosså JH, Fredriksen S . (2005). Fish-macrofauna interactions in a kelp (Laminaria hyperborea) forest. J Mar Biol Assoc UK 85: 1279–1286.
Norderhaug KM, Fredriksen S, Nygaard K . (2003). Trophic importance of Laminaria hyperborea to kelp forest consumers and the importance of bacterial degradation to food quality. Mar Ecol Prog Ser 255: 135–144.
Oksanen J, Blanchet GF, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. (2011). vegan: Community Ecology Package. R package version 2.0-2. http://CRAN.R-project.org/package=vegan.
Östman Ö, Drakare S, Kritzberg ES, Langenheder S, Logue JB, Lindström ES . (2010). Regional invariance among microbial communities. Ecol Lett 13: 118–127.
Pedros-Alio C . (2006). Marine microbial diversity: can it be determined? Trends Microbiol 14: 257–263.
Peter H, Beier S, Bertilsson S, Lindström ES, Langenheder S, Tranvik LJ . (2011). Function-specific response to depletion of microbial diversity. ISME J 5: 351–361.
Pielou EC . (1977) Mathematical Ecology. Wiley: New York.
Pollard PC, Moriarty DJW . (1984). Validity of the tritiated thymidine method for estimating bacterial growth rates: Measurement of isotope dilution during DNA synthesis. Appl Environ Microb 48: 1076–1083.
Quince C, Curtis TP, Sloan WT . (2008). The rational exploration of microbial diversity. ISME J 2: 997–1006.
Quince C, Lanzén A, Davenport RJ, Turnbaugh PJ . (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria, ISBN 3-900051-07-0, URL: http://www.R-project.org.
Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283–290.
Sass H, Koepke B, Ruetters H, Feuerlein T, Droege S, Cypionka H et al. (2010). Tateyamaria pelophila sp nov., a facultatively anaerobic alphaproteobacterium isolated from tidal-flat sediment, and emended descriptions of the genus Tateyamaria and of Tateyamaria omphalii. Int J Syst Evol Micr 60: 1770–1777.
Shannon CE, Weaver W . (1949) The Mathematical Theory of Communication. University of Illinois Press: Urbana, IL.
Sloan W, Lunn M, Woodcock S, Head I, Nee S et al. (2006). Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8: 732–740.
Staufenberger T, Thiel V, Wiese J, Imhoff JF . (2008). Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64: 65–77.
Steneck R, Graham M, Bourque B, Corbett D, Erlandson J, Estes J et al. (2002). Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29: 436–459.
Tokida J . (1960). Marine algae epiphytic on Laminariales plants. Bull Fac Fisheries Hokkaido Univ 11: 73–105.
Torsvik V, Goksøyr J, Daae FL . (1990). High diversity in DNA of soil bacteria. Appl Environ Microb 56: 782–787.
Wang Q, Garrity GM, Tiedje JM, Cole JR . (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73: 5261–5267.
Ward N, Staley JT, Fuerst JA, Giovannoni S, Schlesner H, Stackebrandt E . (2006). The order planctomycetales, including the genera planctomyces, pirellula, gemmata and isosphaera and the candidatus genera brocadia, kuenenia and scalindua. Prokaryotes 7: 757–793.
Woebken D, Teeling H, Wecker P, Dumitriu A, Kostadinov I, DeLong EF et al. (2007). Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. ISME J 1: 419–435.
Acknowledgements
We thank Tomas Sørlie for superb assistance during sampling, Professor Janet Jansson for valuable discussions, Morten Skage for excellent pyrosequencing advice and Kjell Magnus Norderhaug and Trine Bekkby for providing the wave exposure map. The sequencing service was provided by the Norwegian Sequencing Centre (www.sequencing.uio.no), a national technology platform hosted by the University of Oslo and supported by the ‘Functional Genomics’ and ‘Infrastructure’ programs of the Research Council of Norway and the Southeastern Regional Health Authorities. This study was funded by a scholarship awarded to MMB by Egil and Sunniva Baardseths legat and was also financially supported by FMC Biopolymer.
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Bengtsson, M., Sjøtun, K., Lanzén, A. et al. Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6, 2188–2198 (2012). https://doi.org/10.1038/ismej.2012.67
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DOI: https://doi.org/10.1038/ismej.2012.67
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