Abstract
The importance of heterotrophic bacteria relative to phytoplankton in the uptake of ammonium and nitrate was studied in Mediterranean coastal waters (Thau Lagoon) during autumn, when the Mediterranean Sea received the greatest allochthonous nutrient loads. Specific inhibitors and size-fractionation methods were used in combination with isotopic 15N tracers. NO3 − and NH4 + uptake was dominated by phytoplankton (60 % on average) during the study period, which included a flood event. Despite lower biomass specific NH4 + and NO3 uptake rates, free-living heterotrophic bacteria contributed significantly (>30 %) to total microbial NH4 + and NO3 − uptake rates in low chlorophyll waters. Under these conditions, heterotrophic bacteria may be responsible for more than 50 % of primary production, using very little freshly produced phytoplankton exudates. In low chlorophyll coastal waters as reported during the present 3-month study, the heterotrophic bacteria seemed to depend to a greater extent on allochthonous N and C substrates than on autochthonous substrates derived from phytoplankton.
Similar content being viewed by others
References
Berrouard M (2011) Contribution des bactéries hétérotrophes au cycle marin de l'azote dans l'océan Arctique canadien. M. Sc. thesis, University of Laval, Quebec, Canada. pp 54
Bell RT (1990) An explanation for the variability in the conversion factor deriving bacterial cell production from incorporation of [3H] thymidine. Limnol Oceanogr 35:910–913
Bradley PB, Lomas MW, Bronk DA (2010) Inorganic and organic nitrogen use by phytoplankton along Chesapeake Bay, measured using a flow cytometric sorting approach. Estuar Coast Shelf Sci 33:971–984
Chu Y, Salles C, Tournoud M-G, Got PO, Troussellier M, Rodier C, Caro A (2011) Faecal bacterial loads during flood events in Northwestern Mediterranean coastal rivers. J Hydrol 405:501–511
Collos Y, Vaquer A, Bibent B, Souchu P, Slawyk G, Garcia N (2003) Response of coastal phytoplankton to ammonium and nitrate pulses: seasonal variations of nitrogen uptake and regeneration. Aquat Ecol 37:227–236
Dortch O, Thompson PA, Harrison PJ (1991) Short-term interaction between nitrate and ammonium uptake in Thalassiosira-pseudonana—effect of preconditioning nitrogen-source and growth-rate. Mar Biol 110(2):183–193
Dugdale RC, Wilkerson FP (1986) The use of n-15 to measure nitrogen uptake in eutrophic oceans—experimental considerations. Limnol Oceanogr 31(4):673–689
Fisher NS, Cowdell RA (1982) Growth of marine planktonic diatoms on inorganic and organic nitrogen. Mar Biol 72:147–155
Fouilland E, Descolas-Gros C, Collos Y, Vaquer A, Souchu P, Gasc A, Bibent B, Pons V (2002) Influence of nitrogen enrichment on size-fractionated in vitro carboxylase activities of phytoplankton from Thau Lagoon (Coastal Mediterranean Lagoon, France). J Exp Mar Biol Ecol 275(2):147–171
Fouilland E, Gosselin M, Rivkin RB, Vasseur C, Mostajir B (2007) Nitrogen uptake by heterotrophic bacteria and phytoplankton in Arctic surface waters. J Plankton Res 29(4):369–376
Fouilland E, Mostajir B (2010) Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwaters, transitional, coastal and oceanic waters. FEMS Microbiol Ecol 73:419–429
Fouilland E, Mostajir B (2011) Complementary support for the new ecological concept of ‘bacterial independence’ on contemporary phytoplankton production’ in oceanic waters. FEMS Microbiol Ecol 78:206–207
Fouilland E, Trottet A, Bancon-Montigny C, Bouvy M, Le Floc'h E, Gonzalez JL, Hatey E, Mas S, Mostajir B, Nouguier J, Pecqueur D, Rochelle-Newall E, Rodier C, Roques C, Salles C, Tournoud M-G, Vidussi F (2012) Impact of a river flash flood on microbial carbon and nitrogen production in a Mediterranean Lagoon (Thau Lagoon, France). Estuar Coast Shelf Sci 113:192–204
Fouilland E, Tolosa I, Bonnet D, Bouvier C, Bouvier T, Bouvy M, Got P, Le Floc’h E, Mostajir B, Roques C, Sempéré R, Sime-Ngando T, Vidussi F (2014) Bacterial carbon dependence on freshly produced phytoplankton exudates under different nutrient availability and grazing pressure conditions in coastal marine waters. FEMS Microbiol Ecol 87:757–769
Harrison WG (1993) Nutrient recycling in production experiments. ICES Mar Sci Symp 197:149–158
Holmes RM, Aminot A, Kérouel R, Bethanie A, Hooher A, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Aquat Sci 56:1801–1808
Kirchman DL (Ed.) (2000) Microbial ecology of the oceans. Wiley-Liss 542 p
Kirchman DL, Wheeler PA (1998) Uptake of ammonium and nitrate by heterotrophic bacteria and phytoplankton in the sub-Arctic Pacific. Deep-Sea Res I 45:347–365
Lee S, Fuhrman JA (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53:1298–1303
Mackey MD, Mackey DJ, Higgins HW, Wright SW (1996) CHEMTAX—a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar Ecol Prog Ser 144:265–283
Middelburg JJ, Nieuwenhuize J (2000) Uptake of dissolved nitrogen in turbid, tidal estuaries. Mar Ecol Prog Ser 192:79–88
Middelburg JJ, Nieuwenhuize J (2000) Nitrogen uptake by heterotrophic bacteria and phytoplankton in the nitrate-rich Thames estuary. Mar Ecol Prog Ser 203:13–21
Moran XAG, Estrada M, Gasol JM, Pedros-Alio C (2002) Dissolved primary production and the strength of phytoplankton–bacterioplankton coupling in contrasting marine regions. Microb Ecol 44:217–223
Nayar S, Chou LM (2003) Relative efficiencies of different filters in retaining phytoplankton for pigment and productivity studies. Estuar Coast Shelf Sci 58:241–248
Pecqueur D, Vidussi F, Fouilland E, Le Floc’h E, Mas S, Roques C, Salles C, Tournoud M-G, Mostajir B (2011) Dynamics of microbial planktonic food web components during a river flash flood in a Mediterranean coastal lagoon. Hydrobiologia 673:13–27
Plus M, La Jeunesse I, Bouraoui F, Zaldivar J-M, Chapelle A, Lazure P (2006) Modelling water discharged and nitrogen inputs into a Mediterranean lagoon: impact on the primary production. Ecol Model 193:69–89
Rodrigues RMNV, Williams PJL (2002) Inorganic nitrogen assimilation by picoplankton and whole plankton in a coastal ecosystem. Limnol Oceanogr 47(6):1608–1616
Smith DC, Azam F (1992) A simple economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114
Strickland JDH, Parsons TR (1968) Determination of reactive nitrite. In: A practical handbook of seawater analysis. Fish Res Board Can Bull 167:71–75
Tournoud MG, Payraudeau S, Cernesson F, Salles C (2006) Origins and quantification of nitrogen inputs into a coastal lagoon: application to the Thau Lagoon (France). Ecol Model 193:9–33
Tréguer P, Le Corre P (1975) Handbook of seawater nutrient analyses. Autoanalyser II Technicon user guide (2nd ed), Université de Bretagne Occidentale, Laboratoire de Chimie marine, Brest, France, pp. 1–110
Trottet A, Fouilland E, Leboulanger C, Lanouguère E, Bouvy M (2011) Use of inhibitors for coastal bacteria and phytoplankton: application to nitrogen uptake rates. Estuar Coast Shelf Sci 93:151–159
Vaquer A, Troussellier M, Courties C, Bibent B (1996) Standing stock and dynamics of picophytoplankton in the Thau Lagoon (northwest Mediterranean coast). Limnol Oceanogr 41:1821–1828
Veuger B, Middelburg J, Boschker H, Nieuwenhuize J, Rijswijk P, Rochelle- Newall E, Navarro N (2004) Microbial uptake of dissolved organic and inorganic nitrogen in Randers Fjord. Estuar Coast Shelf Sci 61:507–515
Vidussi F, Marty JC, Chiavérini J (2000) Phytoplankton pigment variations during the transition from spring bloom to oligotrophy in the north-western Mediterranean Sea. Deep-Sea Res 47:423–445
Vidussi F, Mostajir B, Fouilland E, Le Floc’h E, Nouguier J, Roques C, Got P, Thibault-Botha D, Bouvier T, Troussellier M (2011) Effects of experimental warming and increased ultraviolet-B radiation on the Mediterranean plankton food web. Limnol Oceanogr 56:206–218
Wheeler PA, Kirchman DL (1986) Utilization of inorganic and organic nitrogen by bacteria in marine systems. Limnol Oceanogr 31:998–1009
Yuan XC, Glibert PM, Xu J, Liu H, Chen MR, Liu HB, Yin KD, Harrison PJ (2012) Inorganic and organic nitrogen uptake by phytoplankton and bacteria in Hong Kong waters. Estuar Coasts 35(1):325–334
Zapata M, Rodríguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45
Acknowledgments
This study was part of the RESTHAU project (2007–2010) “Impact of river loadings on microbial communities from Thau Lagoon” funded by the national EC2CO program and coordinated by E. Fouilland. A. Trottet received a postdoctoral fellowship from The University of Montpellier II. We would like to thank M. Cantou (SMEL, UM2) for his assistance during sampling, P. Raimbault (LMGEM—UMR 6117, Campus de Luminy, Marseilles) for performing the stable isotope analyses and IFREMER Sète for providing us with the solar radiation data. We thank the two reviewers for their constructive and valuable comments, which helped us to improve the manuscript. This project used the facilities of the Mediterranean Center of Marine Ecosystem Experimental Research MEDIMEER funded by UMR 5119 ECOSYM “Ecologie des Systèmes Marins Côtiers”, CNRS Institute of Ecology and Environment (InEE), University of Montpellier 2, IFR 129 Armand Sabatier, CNRS-GDR2476 Réseaux Trophiques Aquatiques, and Région Languedoc-Roussillon.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Trottet, A., Leboulanger, C., Vidussi, F. et al. Heterotrophic Bacteria Show Weak Competition for Nitrogen in Mediterranean Coastal Waters (Thau Lagoon) in Autumn. Microb Ecol 71, 304–314 (2016). https://doi.org/10.1007/s00248-015-0658-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-015-0658-8