Sequential resuspension of biofilm components (viruses, prokaryotes and protists) as measured by erodimetry experiments in the Brouage mudflat (French Atlantic coast)

Journal of Sea Research

Volumn 92, Issue , 2014, Pages 56-65

  Dupuy, Christine ^a   Mallet, Clarisse ^b   Guizien, Katell ^c   Montanié, Hélène ^a   Bréret, Martine ^a   Mornet, Françoise ^d   Fontaine, Camille ^a   Nérot, Caroline ^a,e   Orvain, Francis ^f  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b UNIVERSITÉ BLAISE PASCAL   (France)

^c LABORATOIRE ARAGO   (France)

^d IFREMER   (France)

^e INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

^f UNIVERSITÉ DE CAEN   (France)

Author keywords

Benthic pelagic coupling; Microorganisms; Mudflat; Resuspension; Spatial distribution; Viruses

Indexed keywords

BENTHIC-PELAGIC COUPLING; BIOEROSION; BIOFILM; BIOMASS; CHLOROPHYLL A; MICROORGANISM; MUDFLAT; NEW RECORD; PHYTOBENTHOS; RESUSPENSION; SPATIAL DISTRIBUTION; TIDAL CYCLE;

ATLANTIC COAST [EUROPE]; ATLANTIC COAST [FRANCE]; BROUAGE; CHARENTE MARITIME; FRANCE; POITOU-CHARENTES;

EID: 84907140949     PISSN: 13851101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.seares.2013.12.002     Document Type: Article

References (75)

1. Aminot A., Chaussepied M. Manuel des analyses chimiques en milieu marin 1983, CNEXO, Brest.
2. Andersen T.J., Lanaru M., van Bernem C., Pejrup M., Riethmueller R. Erodibility of a mixed mudflat dominated by microphytobenthos and Cerastoderma edule, East Frisian Wadden Sea, Germany. Estuar. Coast. Shelf Sci. 2010, 87:197-206.
3. Austen I., Andersen T.J., Edelvang K. The influence of benthic diatoms and invertebrates on the erodibility of an intertidal mudflat, the Danish Wadden Sea. Estuar. Coast. Shelf Sci. 1999, 49:99-111.
4. Bak R.P.M., Nieuwland G. Seasonal fluctuations in benthic protozoan populations at different depths in marine sediments. Neth. J. Sea Res. 1989, 24:37-44.
5. Bassoulet P., Le Hir P., Gouleau R., Robert S. Sediment transport over an intertidal mudflat: field investigations and estimation of fluxes within the "Baie de Marennes-Oléron" (France). Cont. Shelf Res. 2000, 20:1635-1653.
6. Blanchard G.F., Cariou-Le Gall V. Photosynthetic characteristics of microphytobenthos in Marennes-Oleron Bay, France: preliminary results. J. Exp. Mar. Biol. Ecol. 1994, 182:1-14.
7. Blanchard G.F., Sauriau P.-G., Cariou-Le Gall V., Gouleau D., Garet M.-J., Olivier F. Kinetics of tidal resuspension of microbiota: testing the effects of sediment cohesiveness and bioturbation using flume experiments. Mar. Ecol. Prog. Ser. 1997, 151:17-25.
8. Blanchard G.F., Guarini J.M., Provot L., Richard P., Sauriau P.G. Measurement of ingestion rate of Hydrobia ulvae (Pennant) on intertidal epipelic microalgae: the effect of mud snail density. J. Exp. Mar. Biol. Ecol. 2000, 255:247-260.
9. Blanchard G.F., Guarini J.M., Orvain F., Sauriau P.G. Dynamic behaviour of benthic microalgal biomass in intertidal mudflat. J. Exp. Mar. Biol. Ecol. 2001, 264:85-100.
10. Breitbart M., Felts B., Kelley S., Mahaffy J., Nulton J., Salamon P., Rohwer F. Diversity and population structure of a near-shore marine-sediment viral community. Proc. R. Soc. Lond. B 2004, 271:565-574.
11. Brinkhoff T., Santegoeds C.M., Sahm K., Kuever J., Muyzer G. A polyphasic approach to study the diversity and vertical distribution of sulfur-oxidizing Thiomicrospira species in coastal sediments of the German Wadden Sea. Appl. Environ. Microbiol. 1998, 64:4650-4657.
12. Brotas V., Cabrita T., Portugal A., Serôdio J., Catarino F. Spatio-temporal distribution of the microphytobenthic biomass in intertidal flats of Tagus Estuary (Portugal). Hydrobiologia 1995, 300-301:93-104.
13. Christiansen C., Vølund G., Lund-Hansen L.C., Bartholdy J. Wind influence on tidal flat sediment dynamics: field investigations in the Ho Bugt, Danish Wadden Sea. Mar. Geol. 2006, 235:75-86.
14. De Backer A., Van Colen C., Vincx M., Degraer S. The role of biophysical interactions within the Yzermonding tidal flat sediment dynamics. Cont. Shelf Res. 2010, 30:1166-1179.
15. de Brouwer J.F.C., Bjelic S., de Deckere E.M.G.T., Stal L.J. Interplay between biology and sedimentology in a mudflat (Biezelingse Ham, Westerschelde, The Netherlands). Cont. Shelf Res. 2000, 20:1159-1177.
16. de Brouwer J.F.C., Wolfstein K., Ruddy G.K., Jones T.E.R., Stal L.J. Biogenic stabilization of intertidal sediments: the importance of extracellular polymeric substances produced by benthic diatoms. Microb. Ecol. 2005, 49:501-512.
17. De Jonge V.N., Colijn F. Dynamics of microphytobenthos biomass in the Ems estuary. Mar. Ecol. Prog. Ser. 1994, 104:185-196.
18. Decho A.W. Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 2000, 20:1257-1273.
19. Drake L.A., Choil K.H., Haske A.G.E., Dobbs F.C. Vertical profiles of virus-like particles and bacteria in the water column and sediments of Chesapeake Bay, USA. Aquat. Microb. Ecol. 1998, 16:17-25.
20. Du G.Y., Son M., An S., Chung I.K. Temporal variation in the vertical distribution of microphytobenthos in intertidal flats of the Nakdong River estuary, Korea. Estuar. Coast. Shelf Sci. 2010, 86:62-70.
21. Dupuy C., Le Gall S., Hartmann H.J., Bréret M. Retention of ciliates and flagellates by the oyster Crassostrea gigas in French Atlantic coastal ponds: protists as a trophic link between bacterioplankton and benthic suspension-feeders. Mar. Ecol. Prog. Ser. 1999, 177:165-175.
22. Epstein S.S. Simultaneous enumeration of protozoa and micrometazoa from marine sandy sediments. Aquat. Microb. Ecol. 1995, 9:219-227.
23. Fenchel T. The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliated protozoa. Ophelia 1969, 6:1-182.
24. Garstecki T., Wickham S.A., Arndt H. Effects of experimental sediment resuspension on a coastal planktonic microbial food web. Estuar. Coast. Shelf Sci. 2002, 55:751-762.
25. Gasol J.M. Benthic flagellates and ciliates in fine freshwater sediments: calibration of a live counting procedure and estimation of their abundances. Microb. Ecol. 1993, 25:247-262.
26. Gerba, C. P., 1984. Applied and theoretical aspects of virus adsorption to surfaces, 30: 133-168. In Advances in Applied Microbiology [ed.], Academic Press, Inc.
27. Giere O. Meiobenthology. The microscopic fauna in aquatic sediments 1993, (328 pp.).
28. Guizien K., Orvain F., Duchêne J.C., Le Hir P. Accounting for rough bed friction factors of mud beds as a result of biological activity in erosion experiments. J. Hydraul. Eng. 2012, 138:979-984.
29. Guizien K., Dupuy C., Ory P., Montanie H., Hartmann H., Chatelain M., Karpytchev M. Microorganism dynamics during a rising tide: disentangling effects of resuspension and mixing with offshore waters above an intertidal mudflat. J. Mar. Syst. 2013, 129:178-188.
30. Haubois A.G., Sylvestre F., Guarini J.M., Richard P., Blanchard G.F. Spatio-temporal structure of the epipelic diatom assemblage from an intertidal mudflat in Marennes-Oléron Bay, France. Estuar. Coast. Shelf Sci. 2005, 64:385-394.
31. 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.
32. Herman P.M.J., Middelburg J.J., Heip C.H.R. Benthic community structure and sediment processes on an intertidal flat: results from the ECOFLAT project. Cont. Shelf Res. 2001, 21(18-19):2055-2071.
33. Honeywill C., Paterson D.N., Hagerthey S.E. Determination of microphytobenthic biomass using pulse-amplitude modulated minimum fluorescence. Eur. J. Phycol. 2002, 37:485-492.
34. Kahl A. Urtiere oder protozoa. Die Tierwelt Deutschlands und der angrenzenden Meeresteile. (J Gustav Fischer, Ed.) 1931, F. Dahl, M. Dahl, H. Bischoff (Eds.).
35. Koh C.H., Khim J.S., Araki H., Yamanishi H., Mogi M., Koga K. Tidal resuspension of microphytobenthic chlorophyll a in a Nanaura mudflat, Saga, Ariake Sea, Japan: flood-ebb and spring-neap variations. Mar. Ecol. Prog. Ser. 2006, 312:85-100.
36. Le Hir P., Cann P., Jestin H., Bassoulet P. Instrumentation légère pour la mesure de l'érodabilité des sédiments vaseux ou sablovaseux. Proc. IXémes Journées Nationales Génie CÔtier-Génie Civil 2006, PARALIA, Nantes, France (in French).
37. Lee J., Hutner S., Bovee E. An Illustrated Guide to the Protozoa (S of Protozoologists, Ed.) 1985.
38. Lorenzen C.J. A method for the continuous measurement of in vivo chlorophyll concentration. Deep-Sea Res. 1966, 13:223-227.
39. Lucas C.H., Widdows J., Brinsley M.D., Salkeld P.N., Herman P.M.J. Benthic pelagic exchange of microalgae at a tidal flat. 1. Pigment analysis. Mar. Ecol. Prog. Ser. 2000, 196:59-73.
40. Macintyre H.L., Geider R.J., Miller D.C. Microphytobenthos: the ecological role of the 'secret garden' of unvegetated, shallow-water marine habitats. 1. Distribution, abundance and primary production. Estuaries 1996, 19:186-201.
41. Malits A., Weinbauer M.G. Effect of turbulence and viruses on prokaryotic cell size, production and diversity. Aquat. Microb. Ecol. 2009, 54:243-254.
42. Mallet C., Agogué H., Bonnemoy F., Guizien K., Orvain F., Dupuy C. Structures of benthic prokaryotic communities and their hydrolytic enzyme activities resuspended from samples of intertidal mudflats: An experimental approach. J. Sea Res. 2013, 92:158-169. (in this issue).
43. Méléder V., Barillé L., Rincé Y., Morançais M., Rosa P., Gaudin P. Spatio-temporal changes in microphytobenthos structure analysed by pigment composition in a macrotidal flat (Bourgneuf Bay, France). Mar. Ecol. Prog. Ser. 2005, 297:83-99.
44. Miller D.C., Geider R.J., Hugh L., Macintyre H.L. Microphytobenthos: the ecological role of the "secret garden" of unvegetated, shallow-water marine habitats. II. Role in sediment stability and shallow-water food webs. Estuaries 1996, 19:202-212.
45. Mitbavkar S., Anil A.C. Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: influence of irradiance and tides. Mar. Biol. 2004, 145:9-20.
46. Montserrat F., Van Colen C., Degraer S., Ysebaert T., Herman P.M.J. Benthic community-mediated sediment dynamics. Mar. Ecol. Prog. Ser. 2008, 372:43-59.
47. Noble R.T., Fuhrman J.A. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 1998, 14:113-118.
48. Orvain F., Sauriau P.G., Sygut A., Joassard L., Le Hir P. Interacting effects of Hydrobia ulvae bioturbation and microphytobenthos on the erodibility of mudflat sediments. Mar. Ecol. Prog. Ser. 2004, 278:205-223.
49. Orvain F., Sauriau P.G., Le Hir P., Guillou G., Cann P., Paillard M. Spatio-temporal variations in intertidal mudflat erodability: Marennes-Oléron Bay, western France. Cont. Shelf Res. 2007, 27:1153-1173.
50. Orvain F., Lefebvre S., Montepini J., Sébire M., Gangnery A., Sylvand B. Spatial and temporal interaction between sediment and microphytobenthos in a temperate estuarine macro-intertidal bay. Mar. Ecol. Prog. Ser. 2012, 458:53-68.
51. Orvain F., Guizien K., Lefebvre L., Bréret M., Dupuy C. Relevance of macrozoobenthic grazers to understand the dynamic behaviour of sediment erodibility and microphytobenthos resuspension in sunny summer conditions. J. Sea Res. 2013, 92:46-55. (in this issue).
52. Pascal P.Y., Dupuy C., Richard P., Mallet C.Armynot, du Châtelet E., Niquil N. Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol. Oceanogr. 2009, 54:1048-1059.
53. Paterson D.M. The migratory behaviour of diatom assemblages in a laboratory tidal micro-ecosystem examined by low temperature scanning electron microscopy. Diatomol. Res. 1986, 1:227-239.
54. Paterson D.M. Short-term changes in the erodibility of intertidal cohesive sediments related to the migratory behaviour of epipelic diatoms. Limnol. Oceanogr. 1989, 34:223-234.
55. Paterson D.M., Tolhurst T.J., Kelly J.A., Honeywill C., Deckere E.M.G., Huet V., Shayler S.A., Black K.S., de Brouwer J.D., Davidson I. Variations in sediment properties, Skeffling mudflat, Humber Estuary, UK. Cont. Shelf Res. 2000, 20:1373-1396.
56. Ricard M. Atlas du Phytoplancton Marin, vol. 2. (CNRS, Eds.) 1987, (Paris).
57. Sahan E., Sabbe K., Creach V., Hernandez-Raquet G., Vyverman W., Stal L.J., Muyzer G. Community structure and seasonal dynamics of diatom biofilms and associated grazers in intertidal mudflats. Aquat. Microb. Ecol. 2007, 47:253-266.
58. Sauer J., Wenderoth K., Maier U.G., Rhield E. Effects of salinity, light and time on the vertical migration of diatom assemblages. Diatomol. Res. 2002, 17:189-203.
59. Serôdio J., Vieira S., Barroso F. Relationship of variable chlorophyll fluorescence indices to photosynthetic rates in microphytobenthos. Aquat. Microb. Ecol. 2007, 49:71-85.
60. Seymour J.R., Seuront L., Doubell P.M., Waters R.L., Mitchell J.G. Microscale patchiness of virioplankton. J. Mar. Biol. Assoc. UK 2006, 86:551-561.
61. Sherr E.B., Caron D.A., Sherr B.F. Staining of heterotrophic protists for visualisation via epifluorescence microscopy. Handbook of Methods in Aquatic Microbial Ecology 1994, 213-227. Lewis Publishers, Boca Raton, FL. P.F. Kemp, B.F. Sherr, E.B. Sherr, J.J. Cole (Eds.).
62. Shimeta J., Sisson J.D. Taxon-specific tidal resuspension of protists into the subtidal benthic boundary layer of a coastal embayment. Mar. Ecol. Prog. Ser. 1999, 177:51-62.
63. Shimeta J., Amos C.L., Beaulieu S.E., Ashiru L.M. Sequential resuspension of protists by accelerating tidal flow: implications for community structure in the benthic boundary layer. Limnol. Oceanogr. 2002, 47:1152-1164.
64. Shimeta J., Amos C.L., Beaulieu S.E., Katz S.L. Resuspension of benthic protists at subtidal coastal sites with differing sediment composition. Mar. Ecol. Prog. Ser. 2003, 259:103-115.
65. 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.
66. Syngouna V.I., Chrysikopoulos C.V. Interaction between viruses and clays in static and dynamic batch system. Environ. Sci. Technol. 2010, 44:4539-4544.
67. Thomsen L., Gust G. Sediment erosion thresholds and characteristics of resuspended aggregates on the western European continental margin. Deep-Sea Res. 2000, 47:1881-1897.
68. Underwood G.J.C. Microphytobenthos and phytoplankton in the Severn estuary, UK: present situation and possible consequences of a tidal energy barrage. Mar. Pollut. Bull. 2010, 61:83-91.
69. Underwood G.J.C., Kromkamp J. Primary production by phytoplankton and microphytobenthos in estuaries. Adv. Ecol. Res. 1999, 29:93-153.
70. 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.
71. Van Colen C., Montserrat F., Vincx M., Herman P.M.J., Ysebaert T., Degraer S. Macrobenthic recovery from hypoxia in an estuarine tidal mudflat. Mar. Ecol. Prog. Ser. 2008, 372:31-42.
72. Van Colen C., Rossi F., Montserrat F., Andersson M.A., Gribsholdt B., Herman P.M.J., Degraer S., Vincx M., Ysebaert T., Middelburg J.J. Organism-sediment interactions govern post-hypoxia recovery of ecosystem functioning. PLoS ONE 2012, 7(11):e49795.
73. Weerman E.J., Van Belzen J., Rietkerk M., Temmerman S., Kefi S., Herman P.M.J., Van De Koppel J. Changes in diatom patch-size distribution and degradation in a spatially self-organized intertidal mudflat ecosystem. Ecology 2012, 93:608-618.
74. Wu Q.L., Chen Y., Xu K., Liu Z., Hahn W.N. Intra-habitat heterogeneity of microbial food web structure under the regime of eutrophication and sediment resuspension in the large subtropical shallow Lake Taihu, China. Hydrobiologia 2007, 581:241-254.
75. Zemb O., Manefield M., Thomas F., Jacquet S. Phage adsorption to bacteria in the light of the electrostatics: a case study using E. coli, T2 and flow cytometry. J. Virol. Methods 2013, 189:283-289.