Bacterial dynamics in a microphytobenthic biofilm: A tidal mesocosm approach

Journal of Sea Research

Volumn 92, Issue , 2014, Pages 36-45

  Agogué, Hélène ^a   Mallet, Clarisse ^b   Orvain, Francis ^c   De Crignis, Margot ^a,c   Mornet, Françoise ^d   Dupuy, Christine ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b UNIVERSITÉ BLAISE PASCAL   (France)

^c UNIVERSITÉ DE CAEN   (France)

^d IFREMER   (France)

Author keywords

Bacteria; Extracellular polymeric substances; Interactions; Mesocosm; Microphytobenthos; Muddy sediment

Indexed keywords

BIOFILM; BIOMASS; CONCENTRATION (COMPOSITION); DISSOLVED ORGANIC CARBON; MESOCOSM; MICROBIAL ACTIVITY; MUDFLAT; PHYTOBENTHOS;

EID: 84907140884     PISSN: 13851101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.seares.2014.03.003     Document Type: Article

References (82)

1. Amin S.A., Parker M.S., Armbrust E.V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 2012, 76:667-684.
2. Amon R.M.W., Benner R. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 1996, 41:41-51.
3. Bellinger B.J., Underwood G.J.C., Ziegler S.E., Gretz M.R. Significance of diatom-derived polymers in carbon flow dynamics within estuarine biofilms determined through isotopic enrichment. Aquat. Microb. Ecol. 2009, 55:169-187.
4. Bhaskar P.V., Grossart H.-P., Bhosle N.B., Simon M. Production of macroaggregates from dissolved exopolymeric substances (EPS) of bacterial and diatom origin. FEMS Microbiol. Ecol. 2005, 53:255-264.
5. Blanchard G.F., Guarini J.M., Orvain F., Sauriau P.G. Dynamic behaviour of benthic microalgal biomass in intertidal mudflats. J. Exp. Mar. Biol. Ecol. 2001, 264:85-100.
6. Boetius A., Lochte K. Regulation of microbial enzymatic degradation of organic matter in deep-sea sediments. Mar. Ecol. Prog. Ser. 1994, 104:299-307.
7. Boetius A., Lochte K. Effect of organic enrichments on hydrolytic potentials and growth of bacteria in deep-sea sediments. Mar. Ecol. Prog. Ser. 1996, 140:239-250.
8. Bratbak G., Dundas I. Bacterial dry matter content and biomass estimations. Appl. Environ. Microbiol. 1984, 48:755-757.
9. Cammen L.M. Annual bacterial production in relation to benthic microalgal production and sediment oxygen uptake in an intertidal sandflat and an intertidal mudflat. Mar. Ecol. Prog. Ser. 1991, 71:13-25.
10. Carpenter S.R. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 1996, 77:677-680.
11. Chin W.-C., Orellana M.V., Verdugo P. Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 1998, 391:568-572.
12. Chiovitti A., Higgins M.J., Harper R.E., Wetherbee R., Bacic A. The complex polysaccharides of the raphid diatom Pinnularia viridis (Bacillariophyceae). J. Phycol. 2003, 39:543-554.
13. Chróst R.J., Overbeck J. Substrate-ectoenzyme interaction: significance of beta-glucosidase activity for glucose metabolism by aquatic bacteria. Arch. Hydrobiol. Adv. Limnol. 1990, 34:93-98.
14. Consalvey M., Paterson D.M., Underwood G.J.C. The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res. 2004, 19:181-202.
15. Cook P.L.M., Veuger B., Böer S., Middelburg J.J. Effect of nutrient availability on carbon and nitrogen incorporation and flows through benthic algae and bacteria in near-shore sandy sediment. Aquat. Microb. Ecol. 2007, 49:165-180.
16. de Brouwer J.F.C., Stal L.J. Short-term dynamics in microphytobenthos distribution and associated extracellular carbohydrates in surface sediments of an intertidal mudflat. Mar. Ecol. Prog. Ser. 2001, 218:33-44.
17. De Brouwer J.F.C., Stal L.J. Daily fluctuations of exopolymers in cultures of the benthic diatoms Cylindrotheca closterium and Nitzschia sp. (Bacillariophyceae). J. Phycol. 2002, 38:464-472.
18. de Jong S., Hofmann P.A.S. Construction and calibration of a rapidly responding pH mini-electrode: application to intertidal sediments. Mar. Ecol. Prog. Ser. 1988, 45:187-192.
19. Decho A.W. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr. Mar. Biol. Annu. Rev. 1990, 28:73-153.
20. Decho A.W. Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 2000, 20:1257-1273.
21. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28:350-356.
22. Fuhrman J.A. Influence of method on the apparent size distribution of bacterioplankton cells: epifluorescence microscopy compared to scanning electron microscopy. Mar. Ecol. Prog. Ser. 1981, 5:103-106.
23. Fuhrman J.A., Azam F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar. Biol. 1982, 66:109-120.
24. Gerbersdorf S., Westrich B., Paterson D. Microbial extracellular polymeric substances (EPS) in fresh water sediments. Microb. Ecol. 2009, 58:334-349.
25. Giroldo D., Vieira A.A.H., Paulsen B.S. Relative increase of deoxy sugars during microbial degradation of an extracellular polysaccharide released by a tropical freshwater Thalassiosira sp. (Bacillariophyceae). J. Phycol. 2003, 39:1109-1115.
26. Gonzales T., Robert-Baudouy J. Bacterial aminopeptidases: properties and functions. FEMS Microbiol. Rev. 1996, 18:319-344.
27. Goto N., Mitamura O., Terai H. Biodegradation of photosynthetically produced extracellular organic carbon from intertidal benthic algae. J. Exp. Mar. Biol. Ecol. 2001, 257:73-86.
28. Grice G.D., Reeve M.R. Marine Mesocosms: Biological and Chemical Research in Experimental Ecosystems 1982, (New York).
29. Guarini J.-M., Blanchard G.F., Gros P., Gouleau D., Bacher C. Dynamic model of the short-term variability of microphytobenthic biomass on temperate intertidal mudflats. Mar. Ecol. Prog. Ser. 2000, 195:291-303.
30. Hamels I., Muylaert K., Casteleyn G., Vyverman W. Uncoupling of bacterial production and flagellate grazing in aquatic sediments: a case study from an intertidal flat. Aquat. Microb. Ecol. 2001, 25:31-42.
31. Hanlon A.R.M., Bellinger B., Haynes K., Xiao G., Hofmann T.A., Gretz M.R., Ball A.S., Osborn A.M., Underwood G.J.C. Dynamics of extracellular polymeric substance (EPS) production and loss in an estuarine, diatom-dominated, microalgal biofilm over a tidal emersion-immersion period. Limnol. Oceanogr. 2006, 51:79-93.
32. Haynes K., Hofmann T.A., Smith C.J., Ball A.S., Underwood G.J.C., Osborn A.M. Diatom-derived carbohydrates as factors affecting bacterial community composition in estuarine sediments. Appl. Environ. Microbiol. 2007, 73:6112-6124.
33. Herlory O., Guarini J.-M., Richard P., Blanchard G.F. Microstructure of microphytobenthic biofilm and its spatio-temporal dynamics in an intertidal mudflat (Aiguillon Bay, France). Mar. Ecol. Prog. Ser. 2004, 282:33-44.
34. Heuer H., Smalla K. Application of denaturing gradient gel electrophoresis and temperature gradient gel electrophoresis for studying soil microbial communities. Modern Soil Microbiology 1997, 353-373. Marcel Dekker, New York. J.D. van Elsas (Ed.).
35. Higgins M.J., Molino P., Mulvaney P., Wetherbee R. The structure and nanomechanical properties of the adhesive mucilage that mediates diatom-substratum adhesion and motility. J. Phycol. 2003, 39:1181-1193.
36. Hoppe H.-G. Attachment of bacteria: advantage or disadvantage for survival in the aquatic environment. Microbial Adhesion and Aggregation 1984, 283-301. Springer-Verlag, Berlin. K.C. Marshall (Ed.).
37. Huston M.A. Microcosm experiments have limited relevance for community and ecosystem ecology: synthesis of comments. Ecology 1999, 80:1088-1089.
38. Kemp W.M., Petersen J.E., Gardner R.H. Scale-dependence and the problem of extrapolation: implications for experimental and natural coastal ecosystems. Scaling Relations in Experimental Ecology 2001, 3-57. University Press, New York, Columbia. R.H. Gardner, W.M. Kemp, V.S. Kennedy, J.E. Petersen (Eds.).
39. King G.M. Characterization of β-glucosidase activity in intertidal marine sediments. Appl. Environ. Microbiol. 1986, 51:373-380.
40. Koroleff F. Direct determination of ammonia in natural waters as indophenol blue. International Council for the Exploration of the Sea 1969, 9:19-22.
41. Lorenzen C.J. A method for the continuous measurement of in vivo chlorophyll concentration. Deep-Sea Res. 1966, 13:223-227.
42. Lowry O.H., Rosenbrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
43. Lubarsky H.V., Hubas C., Chocholek M., Larson F., Manz W., Paterson D.M., Gerbersdorf S.U. The stabilisation potential of individual and mixed assemblages of natural bacteria and microalgae. PLoS ONE 2010, 5:e13794.
44. MacIntyre H., Geider R., Miller D. Microphytobenthos: the ecological role of the "secret garden" of unvegetated shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 1996, 19:186-201.
45. Makk J., Acs E., Marialigeti K., Kovacs G. Investigations on the Danube gravel-biofilm diatom-associated bacterial communities. Biologia 2003, 58:729-742.
46. Mallet C., Debroas D. Relations between organic matter and bacterial proteolytic activity in sediment surface layers of a eutrophic lake (Lake Aydat, Puy de Dome, France). Arch. Hydrobiol. 1999, 145:39-56.
47. Mallet C., Debroas D. Regulation of β- and α-glycolytic activities in the sediments of a eutrophic lake. Microb. Ecol. 2001, 41:106-113.
48. 13C-labeling study. Limnol. Oceanogr. 2000, 45:1224-1234.
49. Orvain F., De Crignis M., Guizien K., Lefebvre S., Mallet C., Takahashi E., Dupuy C. Tidal and Seasonal Effects on the short-term temporal patterns of Bacteria, Microphytobenthos and Exopolymers in Natural Intertidal Biofilms (Brouage, France). J. Sea Res. 2014, 92:6-18. (this issue).
50. Orvain F., Galois R., Barnard C., Sylvestre A., Blanchard G., Sauriau P.G. Carbohydrate production in relation to microphytobenthic biofilm development: an integrated approach in a tidal mesocosm. Microb. Ecol. 2003, 45:237-251.
51. Pascal P.-Y., Dupuy C., Richard P., Mallet C., Châtelet E.A.d., Niquil N. Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol. Oceanogr. 2009, 54:1048-1059.
52. Pesce S., Fajon C., Bardot C., Bonnemoy F., Portelli C., Bohatier J. Effects of the phenylurea herbicide diuron on natural riverine microbial communities in an experimental study. Aquat. Toxicol. 2006, 78:303-314.
53. Petersen J.E., Kemp W.M., Bartleson R., Boynton W.R., Chen C.C., Cornwell J.C., Gardner R.H., Hinkle D.C., Houde E.D., Malone T.C., Mowitt W.R., Murray L., Sanford L.P., Stevenson J.C., Sundberg K.L., Suttles S.E. Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 2003, 53:1181-1197.
54. Pierre G., Graber M., Orvain F., Dupuy C., Maugard T. Biochemical characterization of extracellular polymeric substances extracted from an intertidal mudflat using a cation exchange resin. Biochem. Syst. Ecol. 2010, 38:917-923.
55. Pierre G., Graber M., Rafiliposon B., Dupuy C., Orvain F., Crignis M., Maugard T. Biochemical composition and changes of extracellular polysaccharides (ECPS) produced during microphytobenthic biofilm development (Marennes-Oléron, France). Microb. Ecol. 2012, 63:157-169.
56. Porter K.G., Feig Y.S. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 1980, 25:943-948.
57. Potts M. Desiccation tolerance of prokaryotes. Microbiol. Mol. Biol. Rev. 1994, 58:755-805.
58. Smith D.C., Simon M., Alldredge A.L., Azam F. Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 1992, 359:139-142.
59. Smith D.J., Underwood G.J.C. Exopolymer production by intertidal epipelic diatoms. Limnol. Oceanogr. 1998, 43:1578-1591.
60. Smith D.J., Underwood G.J.C. The production of extracellular carbohydrates by estuarine benthic diatoms: the effects of growth phase and light and dark treatment. J. Phycol. 2000, 36:321-333.
61. Staats N., Stal L.J., De Winder B., Mur L.R. Oxygenic photosynthesis as driving process in exopolysaccharide production of benthic diatoms. Mar. Ecol. Prog. Ser. 2000, 193:261-269.
62. Staats N., Stal L.J., Mur L.R. Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions. J. Exp. Mar. Biol. Ecol. 2000, 249:13-27.
63. Stal L., de Brower J. Biofilm formation by benthic diatoms and their influence on the stabilization of intertidal mudflats. Forschungszentrum Terramare 2003, 12:109-111.
64. Stal L.J., Défarge C. Structure and dynamics of exopolymers in an intertidal diatom biofilm. Geomicrobiol J. 2005, 22:341-352.
65. Sutherland I.W. Polysaccharases for microbial exopolysaccharides. Carbohydr. Polym. 1999, 38:319-328.
66. Sutherland T.F., Grant J., Amos C.L. The effect of carbohydrate production by the diatom Nitzschia curvilineata on the erodibility of sediment. Limnol. Oceanogr. 1998, 43:65-72.
67. Takahashi E., Ledauphin J., Goux D., Orvain F. Optimising extraction of extracellular polymeric substances (EPS) from benthic diatoms: comparison of the efficiency of six EPS extraction methods. Mar. Freshw. Res. 2009, 60:1201-1210.
68. Thornton D.C.O., Kopac S.M., Long R.A. Production and enzymatic hydrolysis of carbohydrates in intertidal sediment. Aquat. Microb. Ecol. 2010, 60:109-125.
69. Tréguer P., Le Corre P., Grall J.R. The seasonal variations of nutrients in the upper waters of the Bay of Biscay region and their relation to phytoplankton growth. Deep-Sea Res. 1979, 26:1121-1152.
70. Underwood G.J.C., Boulcott M., Raines C.A., Waldron K. Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. J. Phycol. 2004, 40:293-304.
71. Underwood G.J.C., Kromkamp J.C. Primary production by phytoplankton and microphytobenthos in estuaries. Adv. Ecol. Res. 1999, 29:93-153.
72. Underwood G.J.C., Paterson D.M. The importance of extracellular carbohydrate production by marine epipelic diatoms. Advances in Botanical Research 2003, 183-240. Academic Press. J.A. Callow (Ed.).
73. Underwood G.J.C., Paterson D.M., Parkes R.J. The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnol. Oceanogr. 1995, 40:1243-1253.
74. van Duyl F.C., De Winder B., Kop A.J., Wollenzien U. Tidal coupling between carbohydrate concentrations and bacterial activities in diatom-inhabited intertidal mudflats. Mar. Ecol. Prog. Ser. 1999, 191:19-32.
75. van Duyl F.C., Kop A.J. Seasonal patterns of bacterial production and biomass in intertidal sediments of the western Dutch Wadden Sea. Mar. Ecol. Prog. Ser. 1990, 59:249-261.
76. Waksman S.A., Butler M.R. Relation of bacteria to diatoms in sea water. J. Mar. Biol. Assoc. U. K. 1937, 22:359-373.
77. Ward J.H. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 1963, 58:236-244.
78. Weerman E.J., van de Koppel J., Eppinga M.B., Montserrat F., Liu Q.-X., Herman P.M.J. Spatial self-organization on intertidal mudflats through biophysical stress divergence. Am. Nat. 2010, 176:15-32.
79. Wellsbury P., Herbert R.A., Parkes J.R. Bacterial activity and production in near-surface estuarine and freshwater sediments. FEMS Microbiol. Ecol. 1996, 19:203-214.
80. Wustman B.A., Gretz M.R., Hoagland K.D. Extracellular matrix assembly in diatoms (Bacillariophyceae): I. A model of adhesives based on chemical characterization and localization of polysaccharides from the marine diatom Achnanthes longipes and other diatoms. Plant Physiol. 1997, 113:1059-1069.
81. Yallop M.L., deWinder B., Paterson D.M., Stal L.J. Comparative structure, primary production and biogenic stabilization of cohesive and non-cohesive marine sediments inhabited by microphytobenthos. Estuar. Coast. Shelf Sci. 1994, 39:565-582.
82. Yallop M.L., Paterson D.M., Wellsbury P. Interrelationships between rates of microbial production, exopolymer production, microbial biomass, and sediment stability in biofilms of intertidal sediments. Microb. Ecol. 2000, 39:116-127.