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Autogenic versus environmental control during development of river biofilm

Published online by Cambridge University Press:  03 April 2009

Armelle Paule ,
Émilie Lyautey ,
Frédéric Garabetian  and
Jean-Luc Rols
Armelle Paule
Affiliation:
Université de Toulouse; UPS, INP; EcoLab (Laboratoire d'Écologie Fonctionnelle); 118 route de Narbonne, 31062 Toulouse, France CNRS; EcoLab; 31062 Toulouse, France
Émilie Lyautey
Affiliation:
Université de Toulouse; UPS, INP; EcoLab (Laboratoire d'Écologie Fonctionnelle); 118 route de Narbonne, 31062 Toulouse, France CNRS; EcoLab; 31062 Toulouse, France
Frédéric Garabetian
Affiliation:
Université de Toulouse; UPS, INP; EcoLab (Laboratoire d'Écologie Fonctionnelle); 118 route de Narbonne, 31062 Toulouse, France CNRS; EcoLab; 31062 Toulouse, France
Jean-Luc Rols*
Affiliation:
Université de Toulouse; UPS, INP; EcoLab (Laboratoire d'Écologie Fonctionnelle); 118 route de Narbonne, 31062 Toulouse, France CNRS; EcoLab; 31062 Toulouse, France
*
[email protected]
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Abstract

In the natural environment, microbial community structure of river biofilm is controlled by biotic and abiotic factors. This study explored the capacity to manipulate the structure of microbial communities by modifying environmental conditions during the course of biofilm development. River epilithic biofilm was cultivated in situ on artificial substrates placed parallel to river water flow. Substrates were incubated for 3 and 5.5 weeks in river to allow natural biofilm development, at two sites with contrasting physico-chemical characteristics. The first site (Auradé, Gers, France) was located in an agricultural watershed basin and the second site (Larroque, Haute-Garonne, France) was located in a forested watershed basin. After 3 weeks of biofilm development, a subset of substrates was collected from one site and transplanted to the second site where they remained for 2.5 further weeks. Epilithic bacterial community structure (at 3 weeks from each site and at 5.5 weeks from biofilms with and without transplantation) was assessed using PCR-DGGE of 16S rDNA fragment. Biofilm biomass was estimated using ash free dry mass (AFDM). After 3 weeks of development, biofilms from the two sites exhibited comparable AFDM values (average of 1.4±0.2 g.m-2). A difference between the two sites was observed after 5.5 weeks of development: AFDM decreased for biofilms from the agricultural watershed basin (from 1.4 to 0.18 g.m-2) as a consequence of grazing pressure (Bithynia), and increased for biofilms from the forested agricultural watershed (from 1.4 to 2.6 g.m-2). Microbial community analyses revealed a differentiated community structure between biofilms from the different sites and exhibited a change of microbial community structure after 5.5 weeks of biofilm development. These observations confirm a process of ecological succession in microbial communities. Changing the incubation site during biofilm development modified the trajectory of these ecological successions, suggesting that site characteristics mainly conditioned the structure of these microbial communities.

Keywords

Colonization experimentcommunity structuregrazingmicrobial ecologysuccession
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 45 , Issue 1 , 2009 , pp. 1 - 10
Copyright
© EDP Sciences, 2009

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References

Anderson-Glenna, M.J., Bakkestuen, V. and Clipson, N.J.W., 2008. Spatial and temporal variability in epilithic biofilm bacterial communities along an upland river gradient. FEMS Microbiol. Ecol. , 64, 407-418. CrossRef
APHA., 1992. Standard methods for the examination of water and wastewater, American Public Health Association, Washington DC.
Araya, R., Tani, K., Takagi, T., Yamaguchi, N. and Nasu, M., 2003. Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol. Ecol. , 43, 111-119. CrossRef
Barbiero, R.P., 2000. A multi-lake comparaison of epilithic diatom communities on natural and artificial substrates. Hydrobiologia , 438, 157-170. CrossRef
Battin, T.J., Kaplan, L.A., Newbold, J.D. and Hansen, C.M.E., 2003. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature , 426, 439-442. CrossRef
Besemer, K., Singer, G., Limberger, R., Chlup, A.K., Hochedlinger, G., Hödl, I., Baranyi, C. and Battin, T.J., 2007. Biophysical controls on community succession in stream biofilms. Appl. Environ. Microbiol. , 73, 4966-4974. CrossRef
Biggs B.J.F., 1996. Patterns in Benthic Algae of Stream. In: Stevenson R.J., Bothwell M.L. and Lowe R.L. (eds.), Algal Ecology - Freshwater Benthic Ecosystem, Academic Press, San Diego, 31-56.
Boston, H.L. and Hill, W.R., 1991. Photosynthesis-light relations of stream periphyton communities. Limnol. Oceanogr. , 36, 644-656. CrossRef
Bothwell, M.L., 1993. Algal-nutrient dynamics. J. N. Amer. Benthol. Soc. , 12, 313-333.
Boulêtreau, S., Garabetian, F., Sauvage, S. and Sanchez-Pérez, J.M., 2006. Assessing the importance of a self-generated detachment process in river biofilm models. Freshwat. Biol. , 51, 901-912. CrossRef
Bourassa, N. and Cattaneo, A., 1998. Control of periphyton biomass in Laurentian streams (Quebec). J. N. Amer. Benthol. Soc. , 17, 420-429. CrossRef
Brümmer, I.H.M., Felske, A.D.M. and Wagner-Döbler, I., 2004. Diversity and seasonal changes of uncultured Planctomycetales in river biofilms. Appl. Environ. Microbiol. , 70, 5094-5101. CrossRef
Burns, A. and Ryder, D.S., 2001. Potential for biofilms as biological indicators in Australian riverine systems. Ecol. Manage. Restor. , 2, 53-63. CrossRef
Cattaneo, A. and Amireault, M.C., 1992. How artificial are artificial substrata for periphyton. J. N. Amer. Benthol. Soc. , 11, 244-256. CrossRef
Chapin, F.S., Zavaleta, E.S., Eviner, E.S., Eviner, V.T., Naylor, R.L., Vitousek, P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., Hobbie, S.E., Mack, M.C. and Diaz, S., 2000. Consequences of changing biodiversity. Nature , 405, 234-242. CrossRef
Cody, D.G., Heath, R.T. and Leff, L.G., 2000. Characterization of benthic bacterial assemblages in a polluted stream using denaturing gradient gel electrophoresis. Hydrobiologia , 432, 207-215. CrossRef
Della Bella, V., Puccinelli, C., Marcheggiani, S. and Mancini, L., 2007. Benthic diatom communities and their relationship to water chemistry in wetlands of central Italy. Ann. Limnol. - Int. J. Lim. , 43, 89-99. CrossRef
DeNicola D.M., 1996. Periphyton responses to temperature at different ecological levels. In: Stevenson R.J., Bothwell M.L. and Lowe R.L. (eds.), Algal Ecology - Freshwater Benthic Ecosystems, Academic Press, San Diego, 149-181.
Devault, D.A., Merlina, G., Lim, P., Probst, J.L. and Pinelli, E., 2007. Multi-residues analysis of pre-emergence herbicides in fluvial sediments: application to the mid-Garonne River. J. Environ. Monitor. , 9, 1009-1017. CrossRef
Dodds, W., 2006. Eutrophication and trophic state in rivers and streams. Limnol. Oceanogr. , 5, 671-680. CrossRef
Dodds, W.K., Jones, J.R. and Welch, E.B., 1997. Suggested classification of stream trophic state: distributions of temperate stream types by chlorophyll, total nitrogen, and phosphorus. Water Res. , 32, 1455-1462. CrossRef
Dorigo, U., Leboulanger, C., Berard, A., Bouchez, A., Humbert, J.F. and Montuelle, B., 2007. Lotic biofilm community structure and pesticide tolerance along a contamination gradient in a vineyard area. Aquat. Microb. Ecol. , 50, 91-102. CrossRef
Dumestre, J.F., Casamayor, E., Massana, R. and Predos-Alio, C., 2002. Changes in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophisation of Petit Saut dam reservoir (French Guiana). Aquat. Microb. Ecol. , 26, 209-221. CrossRef
Eulin, A. and Le Cohu, R., 1998. Epilithic diatom communities during the colonization of artificial substrates in the River Garonne (France). Comparaison with the natural communities. Arch. Hydrobiol. , 143, 79-106. CrossRef
Hill H.L., 1996. Effects of light. In: Stevenson R.J., Bothwell M.L. and Lowe R.L. (eds.), Algal Ecology - Freshwater Benthic Ecosystems, Academic Press, San Diego, 121-148.
Hullar, M.A.J., Kaplan, L.A. and Stahl, D.A., 2006. Recurring seasonal dynamics of microbial communities in stream habitats. Appl. Environ. Microbiol. , 72, 713-722. CrossRef
Jackson, C.R., 2003. Changes in community properties during microbial succession. Oikos , 101, 444-448. CrossRef
Jackson, C.R., Churchill, P.F. and Roden, E.E., 2001. Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology , 82, 555-566. CrossRef
Lane, C.M., Taffs, K.H. and Corfield, J.L., 2003. A comparison of diatom community structure on natural and artificial substrata. Hydrobiologia , 493, 65-79. CrossRef
Lawrence, J.R., Kopf, G., Headley, J.V. and Neu, T.R., 2001. Sorption and metabolism of selected herbicides in river biofilm communities. Can. J. Microbiol. , 47, 634-641. CrossRef
Lawrence, J.R., Swerhone, G.D.W., Wassenaar, L.I. and Nee, T.R., 2005. Effects of selected pharmaceuticals on riverine biofilm communities. Can. J. Microbiol. , 51, 655-669. CrossRef
Lock, M.A., Wallace, R.R., Costerson, J.W., Ventullo, R.M. and Charlton, S.E., 1984. River epilithon: toward a structural-functional model. Oikos , 42, 10-22. CrossRef
Loreau, M., Naeem, S., Inchausti, P., Bengstsson, J., Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D. and Wardle, D.A., 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Ecology , 294, 804-808.
Lyautey, E., Teissier, S., Charcosset, J.Y., Rols, J.L. and Garabetian, F., 2003. Bacterial diversity of epilithic biofilm assemblages of an anthropised river section using DGGE analysis of a 16S rDNA fragment. Aquat. Microb. Ecol. , 33, 217-224. CrossRef
Lyautey, E., Jackson, C.R., Cayrou, J., Rols, J.L. and Garabetian, F., 2005a. Bacterial community succession in natural river biofilm assemblages. Microb. Ecol. , 50, 589-601. CrossRef
Lyautey, E., Lacoste, B., Ten-Hage, L., Rols, J.L. and Garabetian, F., 2005b. Analysis of bacterial diversity in river biofilms using 16S rDNA PCR-DGGE: methodological settings and fingerprints interpretation. Water Res. , 39, 380-388. CrossRef
Manz, W., Wendt-Potthoff, K., Neu, T.R., Szewzyk, U. and Lawrence, J.R., 1999. Phylogenetic composition, spatial structure, and dynamics of lotic bacterial biofilms investigated by fluorescent in situ hybridization and confocal laser scanning microscopy. Microb. Ecol. , 37, 225-237. CrossRef
Morin, S., Duong, T.T., Dabrin, A., Coynel, A., Herlory, O., Baudrimont, M., Delmas, F., Durrieu, G., Schäfer, J., Winterton, P., Blanc, G. and Coste, M., 2008. Long-term survey of heavy-metal pollution, biofilm contamination and diatom community structure in the Riou Mort watershed, South-west France. Environ. Pollut. , 151, 532-542. CrossRef
Murdock, J.N. and Dodds, W.K., 2007. Linking benthic algal biomass to stream substratum topography. J. Phycol. , 43, 449-460. CrossRef
Muyzer, G. and Smalla, K., 1998. Application of denaturing gel electrophoresis (DGGE) temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek , 73, 127-141. CrossRef
Muyzer, G., De Wall, E.C. and Uitterlinden, A.G., 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of PCR-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. , 59, 695-700.
Peterson C.G., 1996. Response of benthic algal communities to natural physical disturbance. In: Stevenson R.J., Bothwell M.L., Lowe R.L. and Thorp J.H. (eds.), Algal Ecology - Freshwater Benthic Ecosystems, Academic Press, San Diego, 375-402.
Prygiel, J. and Coste, M., 1993. The assessment of water quality in the Artois-Picardie water basin (France) by the use of diatom indices. Hydrobiologia , 269, 343-349. CrossRef
Roeselers, G., van Loosdrecht, M. and Muyzer, G., 2007. Heterotrophic pioneers facilitate phototrophic biofilm development. Microb. Ecol. , 54, 578-585. CrossRef
Romani, A.M., Guasch, H., Munoz, I., Ruana, J., Vilalta, E., Schwartz, T., Emtiazi, F. and Sabater, S., 2004. Biofilm structure and function and possible implications for riverine DOC dynamics. Microb. Ecol. , 47, 316-328. CrossRef
Sabater, S., Guasch, H., Romani, A. and Munoz, I., 2002. The effect of biological factors on the efficiency of river biofilms in improving water quality. Hydrobiologia , 469, 149-156. CrossRef
Sabater, S., Guasch, H., Ricart, M., Romani, A., Vidal, G., Klunder, C. and Schmitt-Jansen, M., 2007. Monitoring the effect of chemicals on biological communities. The biofilm as an interface. Anal. Bioanal. Chem. , 387, 1425-1434. CrossRef
Santegoeds, C.M., Ferdelman, T.G., Muyzer, G. and de Beer, D., 1998. Structural and functional dynamics of sulfate-reducing populations in bacterial biofilms. Appl. Environ. Microbiol. , 64, 3731-3739.
Schauer, M., Massana, R. and Pedros-Alio, C., 2000. Spatial differences in bacterioplankton composition along the Catalan coast (NW Mediterranean) assessed by molecular fingerprinting. FEMS Microbiol. Ecol. , 33, 51-59. CrossRef
SCOR-Unesco., 1966. Determination of photosynthetic pigments in sea water. Monogr. Oceanogr. Method Unseco., 1.
Steinman A.D. and Lamberti G.A., 1996. Biomass and pigments of benthic algae. In: Hauer F.R. and Lamberti G.A. (eds.), Stream ecology, Academic Press, San Diego, 295-313.
Stevenson, R.J., 1983. Effects of current and conditions simulating autogenically changing microhabitats on benthic diatom immigration. Ecology , 64, 1514-1524. CrossRef
Teissier, S., Torre, M., Delmas, F. and Garabetian, F., 2007. Detailing biogeochimical N budgets in riverine epilithic biofilms. J. N. Amer. Benthol. Soc. , 26, 178-190. CrossRef
Tlili, A., Dorigo, U., Montuelle, B., Margoum, C., Carluer, N., Gouy, V., Bouchez, A. and Berard, A., 2008. Responses of chronically contaminated biofilms to short pulses of diuron - An experimental study simulating flooding events in a small river. Aquat. Toxicol. , 87, 252-263. CrossRef
Tornes, E., Cambra, J., Goma, J., Leira, M., Ortiz, R. and Sabater, S., 2007. Indicator taxa of benthic diatom communities: a case study in Mediterranean streams. Ann. Limnol. - Int. J. Lim. , 43, 1-11. CrossRef
Van Hannen, E.J., Zwart, G., Van Agterveld, M.P., Gons, H.J., Ebert, J. and Laanbroek, H.J., 1999. Changes in bacterial and eukaryotic community structure after mass lysis of filamentous cyanobacteria associated with viruses. Appl. Environ. Microbiol. , 65, 795-801.
Wetzel R.G. (ed.), 1983. Periphyton of freshwater ecosystem, Dr W. Junk, Boston.