Abstract
This study reports on the factors involved in regulating the composition and structure of bacterial communities epiphytic on intertidal macroalgae, exploring their temporal variability and the role of copper pollution. Culture-independent, molecular approaches were chosen for this purpose and three host species were used as models: the ephemeral Ulva spp. (Chlorophyceae) and Scytosiphon lomentaria (Phaeophyceae) and the long-living Lessonia nigrescens (Phaeophyceae). The algae were collected from two coastal areas in Northern Chile, where the main contrast was the concentration of copper in the seawater column resulting from copper-mine waste disposals. We found a clear and strong effect in the structure of the bacterial communities associated with the algal species serving as host. The structure of the bacterial communities also varied through time. The effect of copper on the structure of the epiphytic bacterial communities was significant in Ulva spp., but not on L. nigrescens. The use of 16S rRNA gene library analysis to compare bacterial communities in Ulva revealed that they were composed of five phyla and six classes, with approximately 35 bacterial species, dominated by members of Bacteroidetes (Cytophaga-Flavobacteria-Bacteroides) and α-Proteobacteria, in both non-polluted and polluted sites. Less common groups, such as the Verrucomicrobiae, were exclusively found in polluted sites. This work shows that the structure of bacterial communities epiphytic on macroalgae is hierarchically determined by algal species > temporal changes > copper levels.
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Andrade S, Moffett J, Correa JA (2006) Distribution of dissolved species and suspended particulate copper in an intertidal ecosystem affected by copper mine tailings in northern Chile. Mar Chem 101:203–212
Andrade S, Pulido MJ, Correa JA (2009) The effect of organic ligands exuded by intertidal seaweeds on copper complexation. Chemosphere 78:397–401
Bohannan B, Hughes J (2003) New approaches to analyzing microbial biodiversity data. Curr Opin Microbiol 6:282–287
Castilla JC (1983) Environmental impact in sandy beaches of copper mine tailings at Chañaral, Chile. Mar Pollut Bull 14:459–464
Castilla JC, Nealler E (1978) Marine environmental impacts due to mining activities of El Salvador copper mine, Chile. Mar Pollut Bull 9:67–70
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 19:117–143
Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Plymouth Marine Laboratory, Plymouth
Correa JA, Lagos NA, Medina MH, Castilla JC, Cerda M, Ramírez M, Martínez E, Faugueron S, Andrade S, Pinto R, Contreras L (2006) Experimental transplants of the large kelp Lessonia nigrescens (Phaeophyceae) in high-energy wave exposed rocky intertidal habitats of northern Chile: experimental, restoration and management applications. J Exp Mar Biol Ecol 335:13–18
Dobretsov SV, Qian PY (2002) Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18:217–228
Dryden CL, Gordon AS, Donat JR (2004) Interactive regulation of dissolved copper toxicity by an estuarine microbial community. Limnol Oceanogr 49:1115–1122
Egan S, Thomas T, Holmström C, Kjelleberg S (2000) Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environ Microbiol 2:343–347
Egan S, James S, Holmström C, Kjelleberg S (2001) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. FEMS Microbiol Ecol 35:67–73
Egan S, Torsten T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219–225
Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28:1971–1985
Guppy R, Bythell JC (2006) Environmental effects on the bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328:133–142
Hellio C, Marechal JP, Veron B, Bremen G, Clare AS, Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany Coast (France). Mar Biotechnol 6:67–82
Hentschel U, Hopke J, Horn M, Friedrich A, Wagner M, Hacker J, Moore B (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440
Lee MR, Correa JA, Zhang H (2002) Effective metal concentrations in porewater and seawater labile metal concentrations associated with copper mine tailings disposal into the coastal waters of the Atacama region of northern Chile. Mar Pollut Bull 44:956–976
Lipson DA (2007) Relationships between temperature responses and bacterial community structure along seasonal and altitudinal gradients. FEMS Microbiol Ecol 59:418–427
Lombardi AT (2000) Copper complexation by cyanophyta and chlorophyta exudates. Phycologia 39:118–135
Longford S, Tujula NA, Crocetti G, Holmes AJ, Holmström C, Kjelleberg S, Steinberg PD, Taylor MW (2007) Comparison of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229
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 52:302–310
Massieux B, Boivin ME, van den Ende FP, Langenskiöld J, Marvan P, Barranguet C, Admiraal W, Laanbroek HJ, Zwart G (2004) Analysis of structural and physiological profiles to assess the effects of Cu on biofilm microbial communities. Appl Environ Microbiol 70:4512–4521
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
Medina M, Andrade S, Faugeron S, Lagos N, Mella D, Correa JA (2005) Biodiversity of rocky intertidal benthic communities associated with copper mine tailing discharges in northern Chile. Mar Pollut Bull 50:396–409
Morán AC, Hengst MB, De la Iglesia R, Andrade S, Correa JA, González B (2008) Changes in bacterial community structure associated with coastal copper enrichment. Environ Toxicol Chem 27:2239–2245
Nylund GM, Pavia H (2005) Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa. Mar Ecol Prog Ser 299:111–121
Osgood MP, Boylen CW (1990) Seasonal variations in bacterial communities in Adirondack streams exhibiting pH gradients. Microb Ecol 20:211–230
Riquelme C, Rojas A, Flores V, Correa JA (1997) Epiphytic bacteria in a copper-enriched environment in Northern Chile. Mar Pollut Bull 34:816–820
Stauber JL, Andrade S, Ramírez M, Adams M, Correa JA (2005) Copper bioavailability in a coastal environment of northern Chile: comparison of bioassay and analytical speciation approaches. Mar Pollut Bull 50:1363–1372
Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629
Stewart FJ, Fritzen CH (2004) Bacteria–algae relationships in Antarctic sea ice. Antarct Sci 16:143–156
Strom S (2008) Microbial ecology of ocean biogeochemistry: a community perspective. Science 320:1043–1045
Tait K, Joint I, Daykin M, Milton DL, Williams P, Cámara M (2005) Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol 7:229–240
Tujula NA, Crocetti GR, Burke C, Thomas T, Holmström C, Kjelleberg S (2009) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J. doi:10.1038/ismej.2009.107
Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438
Webster NS, Bourne D (2007) Bacterial community structure associated with the Antarctic soft coral, Alycyonium antarcticum. FEMS Microbiol Ecol 59:81–94
Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239
Acknowledgments
This study is part of the research program FONDAP 1501 0001 funded by CONICYT, to the Center for Advanced Studies in Ecology & Biodiversity (CASEB) Program 7. Additional support was provided by the Millennium Scientific Initiative through the Millennium Nucleus EMBA grant P/04-007-F; the grants Marine Genomics-CONICYT, FUNDACION ANDES (C-13851), PBCT RED-12, and ICA grant (to JAC). M.B. Hengst was supported by a CONICYT Ph.D. fellowship. We deeply thank to two anonymous referees for their contributions to improve an early version of this paper. Thanks to Jessica Beltran, Carolina Camus, and Alejandra González for their assistance in the field.
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Figure S1
Average values of Richness (up) and Shannon diversity indexes (low) for epiphytic bacterial communities of Ulva, Lessonia, and Scytosiphon, obtained from T-RFLP profiles with MspI endonuclease digestion. The asterisk indicates significant differences between richness values for communities from Scytosiphon with respect to Ulva and Lessonia for algae from Palito 200, obtained with a posteriori Tukey’s test. Diamond, Ulva; square, Lessonia; and triangle, Scytosiphon. PA, Pan de Azúcar; Z, Zenteno; C, Canal; P, Palito 200; and A, Achurra (DOC 31.5 kb)
Table S1
One-way ANOSIM results for comparisons between different sampling periods and localities, from richness, diversity, and evenness values obtained from T-RFLP data digested with MspI, for epiphytic communities associated to Ulva and Lessonia (DOC 38.0 kb)
Table S2
Summary of the two-way crossed ANOSIM test based on Bray–Curtis similarity matrices derived from abundance data square-root transformed to determine the effect of month and copper level on the community structure of bacterial epiphytes associated with Ulva and Lessonia, during 2005 and 2006 (DOC 31.0 kb)
Table S3
Comparisons of epiphytic communities of Lessonia from pristine and copper-polluted sites. Data from T-RFLP were obtained by digestions with HhaI and MspI, and similarity values between sites were obtained with square-root transformed data by SIMPER analysis (DOC 42.0 kb)
Table S4
T-RFs contribution to similarity of epiphytic community structure of Lessonia in pristine and copper-polluted sites, obtained by SIMPER analysis (DOC 80.5 kb)
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Hengst, M.B., Andrade, S., González, B. et al. Changes in Epiphytic Bacterial Communities of Intertidal Seaweeds Modulated by Host, Temporality, and Copper Enrichment. Microb Ecol 60, 282–290 (2010). https://doi.org/10.1007/s00248-010-9647-0
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DOI: https://doi.org/10.1007/s00248-010-9647-0