Abstract
Purpose
Sediment erosion and transport is a governing factor in the ecological and commercial health of aquatic ecosystems from the watershed to the sea. There is now a general consensus that biogenic mediation of submersed sediments contributes significantly to the resistance of the bed to physical forcing. This important ecosystem function has mainly been linked to microalgae (“ecosystem engineers”) and their associated extracellular polymeric substances (EPS), yet little is known about the impact of bacterial assemblages and how their varying interactions with microalgae affect the overall biostabilization potential of the combined community.
Materials and methods
Natural assemblages of bacteria and diatoms—originating from sediment and water samples from the Eden Estuary (Scotland, UK)—were growing on noncohesive glass beads over 5 weeks. The adhesion and the stability of the biofilm was determined by magnetic particle induction (MagPI) and by Cohesive Strength Meter (CSM), respectively, and related to EPS (spectrophotometric determination of carbohydrates and proteins), bacterial cell numbers (flow cytometry), bacterial community (fluorescence in situ hybridization (FISH)), diatom biomass (spectrophotometric determination of chlorophyll a), and diatom assemblage composition (microscopy).
Results and discussion
The adhesive properties and stability of the biofilm were significantly enhanced over time as compared to controls. The diatoms profited from additional nutrients, while bacteria dominated in nutrient-limited cultures. Subsequent shifts in the microbial population at a species level resulted in varying patterns of EPS production which moderated the biostabilization capacity: Cultures with strong diatom development were less stable than cultures dominated by bacteria (MagPI: ×8.5 and ×10.8, CSM: ×2.5 and ×5.7, respectively). The data also suggested synergistic effects between proteins and carbohydrates, which enhanced adhesion and stability.
Conclusions
Bacteria populations under these conditions can be regarded as “ecosystem engineers” since their role in sediment stabilization is more important than previously recognized. Abiotic factors such as nutrients altered the interactions between bacteria and microalgae to influence the overall microbial stabilization potential (“engineering web”) by affecting the quantity and quality of EPS. Data from MagPI and CSM correlated well (R 2 = 0.82, P < 0.0001), and the new technique, MagPI, is to be recommended for studies on growing biofilms since it determines subtle changes in sediment/biofilm properties with high sensitivity.
Recommendations and perspectives
Further studies should examine the highly species-specific interactions between microalgae and bacteria and their effects on EPS secretion to impact stability as well as postentrainment of sediments under varying abiotic scenarios. Our growing understanding of the ecosystem functionality of “bioengineering” will have wider implications for water framework directive and sediment/pollutant management strategies.
Similar content being viewed by others
References
Alldredge AL, Gotschalk CC (1989) Direct observations of the mass flocculation of diatom blooms—characteristics, settling velocities and formation of diatom aggregates. Deep-sea Res, Part 1, Oceanogr Res Pap 36:159–171
Alm EW, Oerther DB, Larsen N, Stahl DA, Raskin L (1996) The oligonucleotide probe database. Appl Environ Microbiol 62:3557–3559
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16 S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925
Boeckelmann U, Manz W, Neu TR, Szewzyk U (2002) Investigation of lotic microbial aggregates by a combined technique of fluorescent in situ hybridization and lectin-binding-analysis. J Microbiol Methods 49:75–87
Boivin MEY, Greve GD, Garcia-Meza JV, Massieux B, Sprenger W, Kraak MHS, Breure AM, Rutgers M, Admiraal W (2007) Algal-bacterial interactions in metal contaminated floodplain sediments. Environ Pollut 145:884–894
Boogert NJ, Paterson DM, Laland KN (2006) The implications of niche construction and ecosystem engineering for conservation biology. Bioscience 56:570–578
Bruckner CG, Bahulikar R, Rahalkar M, Schink B, Kroth PG (2008) Bacteria associated with benthic diatoms from lake constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl Environ Microbiol 74:7740–7749
Commission BMEP (1988) Guidelines for the baltic monitoring programme for the third stage. Loose sheet version of the Baltic Sea Environments Proceedings, pp 16–23
Costerton JW, Geesey GG, Cheng KJ (1978) How bacteria stick. Sci Am 238:86–95
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
Czaczyk K, Myszka K (2007) Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Pol J Environ Stud 16:799–806
Dade WB, Davis JD, Nichols PD, Nowell ARM, Thistle D, Trexler MB, White DC (1990) Effects of bacterial exopolymer adhesion on the entrainment of sand. Geomicrobiol J 8:1–16
Dade WB, Self RL, Pellerin NB, Moffet A, Jumars PA, Nowell ARM (1996) The effects of bacteria on the flow behavior of clay seawater suspensions. J Sediment Res 66:39–42
Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444
Dang HY, Li TG, Chen MN, Huang GQ (2008) Cross-Ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microbiol 74:52–60
Decho AW (1990) Microbial exopolymer secretions in ocean environments—their role(s) in food webs and marine processes. Oceanogr Mar Biol 28:73–153
Defew EC, Paterson DM, Hagerthey SE (2002) The use of natural microphytobenthic assemblages as laboratory model systems. Mar Ecol Prog Ser 237:15–25
Droppo IG, Ross N, Skafel M, Liss SN (2007) Biostabilization of cohesive sediment beds in a freshwater wave-dominated environment. Limnol Oceanogr 52:577–589
Flemming HC, Wingender J (2001a) Relevance of microbial extracellular polymeric substances (EPSs)—Part II: technical aspects. Water Sci Technol 43:9–16
Flemming HC, Wingender J (2001b) Relevance of microbial extracellular polymeric substances (EPSs)—Part I: structural and ecological aspects. Water Sci Technol 43:1–8
Foerstner U, Salomons W (2008) Trends and challenges in sediment research 2008: the role of sediments in river basin management. J Soils Sediments 8:281–283
Friend PL, Ciavola P, Cappucci S, Santos R (2003) Bio-dependent bed parameters as a proxy tool for sediment stability in mixed habitat intertidal areas. Cont Shelf Res 23:1899–1917
Fukami K, Nishijima T, Ishida Y (1997) Stimulative and inhibitory effects of bacteria on the growth of microalgae. Hydrobiologia 358:185–191
Gerbersdorf SU, Jancke T, Westrich B (2005) Physico-chemical and biological sediment properties determining erosion resistance of contaminated riverine sediments—temporal and vertical pattern at the Lauffen reservoir/River Neckar, Germany. Limnologica 35:132–144
Gerbersdorf SU, Jancke T, Westrich B (2007) Sediment properties for assessing the erosion risk of contaminated riverine sites. J Soils Sediments 7:25–35
Gerbersdorf SU, Manz W, Paterson DM (2008) The engineering potential of natural benthic bacterial assemblages in terms of the erosion resistance of sediments. FEMS Microbiol Ecol 66:282–294
Goto N, Mitamura O, Terai H (2001) Biodegradation of photosynthetically produced extracellular organic carbon from intertidal benthic algae. J Exp Mar Biol Ecol 257:73–86
Grossart HP, Simon M, Logan BE (1997) Formation of macroscopic organic aggregates (lake snow) in a large lake: the significance of transparent exopolymer particles, phytoplankton, and zooplankton. Limnol Oceanogr 42:1651–1659
Guerrini F, Mazzotti A, Boni L, Pistocchi R (1998) Bacterial-algal interactions in polysaccharide production. Aquat Microb Ecol 15:247–253
Guo H, Yi W, Song JK, Wang PG (2008) Current understanding on biosynthesis of microbial polysaccharides. Curr Top Med Chem 8:141–151
Haag I, Westrich B (2001) Correlating erosion threshold and physicochemical properties of natural cohesive sediments. Hydraulics of Rivers Water Works and Machinery, Vol 1i, Theme D, Proceedings, pp 84–90
Hilscherova K, Dusek L, Kubik V, Cupr P, Hofman J, Klanova J, Holoubek I (2007) Redistribution of organic pollutants in river sediments and alluvial soils related to major floods. J Soils Sediments 7:167–177
Jain A, Nishad KK, Bhosle NB (2007) Effects of DNP on the cell surface properties of marine bacteria and its implication for adhesion to surfaces. Biofouling 23:171–177
Jansson M (1993) Uptake, exchange, and excretion of orthophosphate in phosphate-starved Scenedesmus quadricauda and Pseudomonas K7. Limnol Oceanogr 38:1162–1178
Jorand F, Boue-Bigne F, Block JC, Urbain V (1998) Hydrophobic/hydrophilic properties of activated sludge exopolymeric substances. Water Sci Technol 37:307–315
Jung SW, Kim BH, Katano T, Kong DS, Han MS (2008) Pseudomonas fluorescens HYK0210-SK09 offers species-specific biological control of winter algal blooms caused by freshwater diatom Stephanodiscus hantzschii. J Appl Microbiol 105:186–195
Klug JL (2005) Bacterial response to dissolved organic matter affects resource availability for algae. Can J Fish Aquat Sci 62:472–481
Krammer K, Lange-Bertalot H (1986-1991) Sueßwasserflora von Mitteleuropa. In: Ettl H, Gerloff J, Heynig D, Mollenhauer D, Ettl H, Gerloff J, Heynig D, Mollenhauer D (eds) Bacillariophyceae. Teil 1–4. Gustav Fischer Verlag, Stuttgart
Lange-Bertalot H (1997) A first ecological evaluation of the diatom flora in Central Europe. Lauterbornia 31:117–123
Larson F, Lubarsky H, Paterson DM, Gerbersdorf SU (2009) Surface adhesion measurements in aquatic biofilms using magnetic particle induction: MagPI. Limnol Oceanogr: Methods 7:490–497
Le Hir P, Monbet Y, Orvain F (2007) Sediment erodability in sediment transport modelling: can we account for biota effects? Cont Shelf Res 27:1116–1142
Liu Y, Fang HHP (2003) Influences of extracellular polymeric substances (EPS) on flocculation, settling, and dewatering of activated sludge. Crit Rev Environ Sci Technol 33:237–273
Lundkvist M, Grue M, Friend PL, Flindt MR (2007) The relative contributions of physical and microbiological factors to cohesive sediment stability. Cont Shelf Res 27:1143–1152
Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria—problems and solutions. Syst Appl Microbiol 15:593–600
Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology-UK 142:1097–1106
Manz W (1999) In situ analysis of microbial biofilms by rRNA-targeted oligonucleotide probing. Biofilms 310:79–91
Marques AM, Estanol I, Alsina JM, Fuste C, Simonpujol D, Guinea J, Congregado F (1986) Production and rheological properties of the extracellular polysaccharide synthesized by Pseudomonas sp strain EPS-5028. Appl Environ Microbiol 52:1221–1223
McNeil J, Lick W (2004) Erosion rates and bulk properties of sediments from the Kalamazoo River. J Great Lakes Res 30:407–418
Neef A (1997) Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. PhD Thesis, Technische Universität, München
Owens PN (2007) Background and summary of this issue on sediment linkages. J Soils Sediments 7:273–276
Pankow H (1990) Ostsee-algenflora. Gustav Fischer Verlag, Jena
Paterson DM (1989) Short-term changes in the erodibility of intertidal cohesive sediments related to the migratory behavior of epipelic diatoms. Limnol Oceanogr 34:223–234
Paterson DM, Tolhurst TJ, Kelly JA, Honeywill C, de Deckere E, Huet V, Shayler SA, Black KS, de Brouwer J, Davidson I (2000) Variations in sediment properties, Skeffling mudflat, Humber Estuary, UK. Cont Shelf Res 20:1373–1396
Pennisi E (2002) Materials science—biology reveals new ways to hold on tight. Science 296:250–251
Rabus R, Fukui M, Wilkes H, Widdel F (1996) Degradative capacities and 16 S rRNA-targeted whole-cell hybridization of sulfate-reducing bacteria in an anaerobic enrichment culture utilizing alkylbenzenes from crude oil. Appl Environ Microbiol 62:3605–3613
Ribalet F, Intertaglia L, Lebaron P, Casotti R (2008) Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. Aquat Toxicol 86:249–255
Roller C, Wagner M, Amann R, Ludwig W, Schleifer KH (1994) In-situ probing of gram-positive bacteria with high DNA G+C content using 235-ribosomal-RNA-targeted Oligonucleotides. Microbiol-SGM 140:2849–2858
Sanin SL, Sanin FD, Bryers JD (2003) Effect of starvation on the adhesive properties of xenobiotic degrading bacteria. Process Biochem 38:909–914
Schaefer H, Abbas B, Witte H, Muyzer G (2002) Genetic diversity of 'satellite' bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol 42:25–35
Simonsen R (1962) Untersuchungen zur Systematik und Ökologie der Bodendiatomeen der westlichen Ostsee. Int Rev Gesamten Hydrobiol. 1:1–44
Slob A, Gerrits L (2007) Sediment linkages between the river catchment and the sea. J Soils Sediments 7:277–284
Staats N, De Winder B, Stal LJ, Mur LR (1999) Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur J Phycol 34:161–169
Stal LJ (2003) Microphytobenthos, their extracellular polymeric substances, and the morphogenesis of intertidal sediments. Geomicrobiol J 20:463–478
Suminto HK (1996) Effects of bacterial coexistence on the growth of a marine diatom Chaetoceros gracilis. Fish Sci 62:40–43
Underwood GJC, Phillips J, Saunders K (1998) Distribution of estuarine benthic diatom species along salinity and nutrient gradients. Eur J Phycol 33:173–183
Underwood GJC, Paterson DM (2003) The importance of extracellular carbohydrate production by marine epipelic diatoms. Adv Bot Res 40(40):183–240
Underwood GJC, Boulcott M, Raines CA, Waldron K (2004) Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. J Phycol 40:293–304
van Duyl FC, de Winder B, Kop AJ, Wollenzien U (1999) Tidal coupling between carbohydrate concentrations and bacterial activities in diatom-inhabited intertidal mudflats. Mar Ecol Prog Ser 191:19–32
Vardy S, Saunders JE, Tolhurst TJ, Davies PA, Paterson DM (2007) Calibration of the high-pressure cohesive strength meter (CSM). Cont Shelf Res 27:1190–1199
Wichard T, Poulet SA, Pohnert G (2005) Determination and quantification of alpha, beta, gamma, delta-unsaturated aldehydes as pentafluorobenzyl-oxime derivates in diatom cultures and natural phytoplankton populations: application in marine field studies. J Chromatogr B 814:155–161
Witkowski A, Lange-Bertalot H, Metzeltin D (2000) Diatom flora of marine coasts I. In: Lange-Bertalot H (ed) Iconographia diatomologica. A. R. G. Gantner Verlag K. G, Ruggell, Liechtenstein, pp 1–925
Acknowledgments
S. U. Gerbersdorf was funded by Marie Curie Individual Fellowship (European Commission, FP6, Project BioMech) and H. Lubarsky by EU research training network (MRTN-CT-2006-035695). R. Bittner was a student of the Lette Verein, Technical School for Chemistry and Biology, Berlin, and supported by the EU transnational traineeship Leonardo-da-Vinci.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Klara Hilscherova
Rights and permissions
About this article
Cite this article
Gerbersdorf, S.U., Bittner, R., Lubarsky, H. et al. Microbial assemblages as ecosystem engineers of sediment stability. J Soils Sediments 9, 640–652 (2009). https://doi.org/10.1007/s11368-009-0142-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-009-0142-5