Skip to main content

Advertisement

Log in

Physiological and photophysiological responses of the benthic diatom Entomoneis paludosa (Bacillariophyceae) to dissolved inorganic and organic nitrogen in culture

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Benthic diatoms are dominant primary producers in intertidal flats. This study investigated the effect of different nitrogen sources and concentrations on Entomoneis paludosa growth and physiological responses. Six nitrogen sources either inorganic (nitrate and ammonium) or organic (urea, arginine, glutamine and glycine) supplied at two concentrations (40 and 400 µM-N) induced significant effects on growth, carbon, nitrogen, pigment content and maximum PSII quantum efficiency (F v /F m). Entomoneis paludosa grew under all nitrogen sources albeit showing differences in lag phase, growth rate and cell yield. Inorganic nitrogen, urea and arginine induced higher growth, whereas glycine did not support high biomass. F v /F m showed variability dependent on nitrogen source and C/N ratio. F v /F m varied between 0.55 and 0.65 at 400 μM-N with the highest values observed in glycine, glutamine and urea, whereas nitrate, ammonium and arginine induced lower F v /F m. All cellular components decreased in the 40 µM-N treatments, with nitrogen and pigments being lower than carbon content. Light-harvesting pigment ratios Chl c/Chl a and photoprotective pigment ratios (diatoxanthin + diadinoxanthin)/Chl a increased, while fucoxanthin/Chl a ratios were unaffected by N-limitations. Entomoneis paludosa was capable of quickly adapting and using a wide variety of nitrogen sources. This adaptability may contribute to microphytobenthos diatom ecological success in mudflat ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Admiraal W (1977) Tolerance of estuarine benthic diatoms to high concentrations of ammonia, nitrite ion, nitrate ion and orthophosphate. Mar Biol 43:307–315

    Article  CAS  Google Scholar 

  • Admiraal W (1984) The ecology of estuarine sediment-inhabiting diatoms. Prog Phycol Res 3:269–322

    Google Scholar 

  • Admiraal W, Laane RWPM, Peletier H (1984) Participation of diatoms in the amino acid cycle of coastal waters; uptake and excretion in cultures. Mar Ecol Prog Ser 15:303–306

    Article  CAS  Google Scholar 

  • Admiraal W, Riaux-Gobin C, Laane RWPM (1987) Interactions of ammonium, nitrate, and D- and L- amino acids in the nitrogen assimilation of two species of estuarine benthic diatoms. Mar Ecol Prog Ser 40:267–273

    Article  CAS  Google Scholar 

  • Allen AE, Vardi A, Bowler C (2006) An ecological and evolutionary context for integrated nitrogen metabolism and related signalling pathways in marine diatoms. Curr Opin Plant Biol 9:264–273

    Article  CAS  Google Scholar 

  • Allen AE, Dupont CL, Obornik M et al (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–207

    Article  CAS  Google Scholar 

  • Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684

    Article  CAS  Google Scholar 

  • Antia NJ, Berland BR, Bonin DJ, Maestrini SY (1975) Comparative evaluation of certain organic and inorganic sources of nitrogen for phototrophic growth of marine microalgae. J Mar Biol Assoc UK 55:519–539

    Article  CAS  Google Scholar 

  • Antia NJ, Harrison PJ, Oliveira L (1991) The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia 30:1–89

    Article  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  Google Scholar 

  • Bates SS, Worms J, Smith JC (1993) Effects of ammonium and nitrate on domoic acid production by Pseudo-nitzschia pungens in batch culture. Can J Fish Aquat Sci 50:1248–1254

    Article  CAS  Google Scholar 

  • Beardall J (1989) Phtosynthesis and photorespiration in marine phytoplankton. Aquat Bot 34:105–130

    Article  CAS  Google Scholar 

  • Beardall J, Young E, Roberts S (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63:44–69

    Article  CAS  Google Scholar 

  • Bender SJ, Parker MS, Armbrust EV (2012) Coupled effects of light and nitrogen source on the urea cycle and nitrogen metabolism over a diel cycle in the marine diatom Thalassiosira pseudonana. Protist 163:232–251

    Article  CAS  Google Scholar 

  • Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110:689–696

    CAS  Google Scholar 

  • Bertrand EM et al (2015) Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci USA 112:9938–9943

    Article  CAS  Google Scholar 

  • Bowler C, Andrew EA, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  Google Scholar 

  • Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331

    Article  CAS  Google Scholar 

  • Brzezinski MA (1985) The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J Phycol 21:347–357

    Article  CAS  Google Scholar 

  • Burdige DJ, Zheng SL (1998) The biogeochemical cycling of dissolved organic nitrogen in estuarine sediments. Limnol Oceanogr 43:1796–1813

    CAS  Google Scholar 

  • Carpenter EJ, Capone DG (1992) Nitrogen fixation in Trichodesmium blooms. In: Carpenter EJ, Capone DG, Rueter J (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer Academic Publishers, The Netherlands, pp 211–217

    Chapter  Google Scholar 

  • Cartaxana P, Ruivo M, Hubas C, Davidson I, Serôdio J, Jesus B (2011) Physiological versus behavioral photoprotection in intertidal epipelic and epipsammic benthic diatom communities. J Exp Mar Biol Ecol 405:120–127

    Article  Google Scholar 

  • Claquin P, Martin-Jezequel V, Kromkamp JC, Veldhuis MJW, Kraay GW (2002) Uncoupling of silicon compared with carbon and nitrogen metabolisms and the role of the cell cycle in continuous cultures of Thalassiosira pseudonana (Bacillariophyceae) under light, nitrogen, and phosphorus control. J Phycol 38:922–930

    Article  CAS  Google Scholar 

  • Cleveland JS, Perry MJ (1987) Quantum yield, relative specific absorption and fluorescence in nitrogen limited Chaetoceros gracilis. Mar Biol 94:489–497

    Article  CAS  Google Scholar 

  • Collos Y, Harrison PJ (2014) Acclimation and toxicity of high ammonium concentrations to unicellular algae. Mar Pollut Bull 80:8–23

    Article  CAS  Google Scholar 

  • Costa C, Dijkema C, Friedrich M, Garcia-Encina P, Fernandez-Polanco F, Stams AJM (2000) Denitrification with methane as electron donor in oxygen-limited bioreactors. Appl Microbiol Biotechnol 53:754–762

    Article  CAS  Google Scholar 

  • Darley MW (1977) Biochemical composition. In: Werner D (ed) The biology of diatoms. University of California press, Berkeley, pp 198–223

    Google Scholar 

  • Doghri I, Rodrigues S, Bazire A, Dufour A, Akbar D, Sopena V, Sable S, Lanneluc I (2015) Marine bacteria from the French Atlantic coast displaying high forming-biofilm abilities and different biofilm 3D architectures. BMC Microbiol. doi:10.1186/s12866-015-0568-4

    Google Scholar 

  • Dortch Q (1982) Effect of growth conditions on accumulation of internal nitrate, ammonium, amino acids and protein in three marine diatoms. J Exp Mar Biol Ecol 61:243–264

    Article  CAS  Google Scholar 

  • Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol Prog Ser 61:183–201

    Article  CAS  Google Scholar 

  • Fisher NS, Cowdell RA (1982) Growth of marine planktonic diatoms on inorganic and organic nitrogen. Mar Biol 72:147–155

    Article  Google Scholar 

  • Flynn KJ, Butler I (1986) Nitrogen sources for the growth of marine microalgae: role of dissolved free amino acids. Mar Ecol Prog Ser 34:281–304

    Article  CAS  Google Scholar 

  • Flynn KJ, Syrett PJ (1985) Development of the ability to take up l-lysine by the diatom Phaeodactylum tricornutum. Mar Biol 89:317–325

    Article  CAS  Google Scholar 

  • Flynn KJ, Syrett PJ (1986) Characteristics of the uptake system for L-lysine and L-arginine in Phaeodactylum tricornutum. Mar Biol 90:151–158

    Article  CAS  Google Scholar 

  • Flynn KJ, Wright CRN (1986) The simultaneous assimilation of ammonium and l-arginine by the diatom Phaeodactylum tricornutum Bohlin. J Exp Mar Biol Ecol 95:257–269

    Article  CAS  Google Scholar 

  • Forster R, Martin-Jézéquel V (2005) Photophysiological variability of microphytobenthic diatoms after growth in different types of culture conditions. Phycologia 44:393–402

    Article  Google Scholar 

  • Geider RJ, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17

    Article  Google Scholar 

  • Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J Phycol 29:755–766

    Article  CAS  Google Scholar 

  • Geng H, Belas R (2010) Molecular mechanisms underlying roseobacter–phytoplankton symbioses. Curr Opin Biotechnol 21:332–338

    Article  CAS  Google Scholar 

  • Glibert PM (1982) Regional studies of daily, seasonal and size fraction variability in ammonium remineralization. Mar Biol 70:209–222

    Article  CAS  Google Scholar 

  • Glibert PM, Azanza R, Burford M et al (2008) Ocean urea fertilization for carbon credits poses high ecological risks. Mar Pollut Bull 56:1049–1056

    Article  CAS  Google Scholar 

  • Goeyens L, Kindermans N, Abu Yusuf M, Elskens M (1998) A room temperature procedure for the manual determination of urea in seawater. Estuar Coast Shelf Sci 47:415–418

    Article  CAS  Google Scholar 

  • Gruber N (2008) The marine nitrogen cycle: overview and challenges. In: Capone DG, Bronk DA, Mulholland MR (eds) Nitrogen in the marine environment. Elsevier, San Diego, pp 1–50

    Chapter  Google Scholar 

  • Guerrini F, Cangini M, Boni L, Trost P, Pistocchi R (2000) Metabolic responses of the diatom Achnanthes brevipes (bacillariophyceae) to nutrient limitation. J Phycol 36:882–890

    Article  CAS  Google Scholar 

  • Guillard RRL (1973) Division rates. In: Stein JR (ed) Handbook of phycological methods. Cambridge University Press, Cambridge, pp 289–312

    Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60

    Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • Guldberg LB, Finster K, Jorgensen NOG, Middelboe M, Lomstein BA (2002) Utilization of marine sedimentary dissolved organic nitrogen by native anaerobic bacteria. Limnol Oceanogr 47:1712–1722

    Article  CAS  Google Scholar 

  • Hammer KD, Kattner G (1986) Dissolved free amino acids in the marine environment: a carbon to nitrogen ratio shift during diatom blooms. Mar Ecol Prog Ser 31:35–45

    Article  CAS  Google Scholar 

  • Hammer KD, Eberlein K, Kattner G, Brockmann UH (1983) Fluctuations of dissolved amino acids: a comparison of natural and enclosed phytoplankton populations in the North Sea. In: Sündermann J (ed) North Sea dynamics. Springer, Berlin, pp 560–572

    Google Scholar 

  • Harrison PJ, Conway HL, Holmes RW, Davis CO (1977) Marine diatoms grown in chemostats under silicate or ammonium limitation. III. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum and Thalassiosira gravida. Mar Biol 43:19–31

    Article  CAS  Google Scholar 

  • Harrison PJ, Thompson PA, Calderwood GS (1990) Effects of nutrient and light limitation on the biochemical composition of phytoplankton. J Appl Phycol 2:45–56

    Article  Google Scholar 

  • Hellebust JA (1978) Uptake of organic substrates by Cyclotella cryptica (Bacillariophyceae): effects of ions, ionophores and meetabolic and transport inhibitors. J Phycol 14:79–83

    Article  CAS  Google Scholar 

  • Hellebust JA, Guillard RRL (1967) Uptake specificity for organic substrates by the marine diatom Melosira nummuloides. J Phycol 3:132–136

    Article  CAS  Google Scholar 

  • Jauffrais T, Drouet S, Turpin V, Méléder V, Jesus B, Cognie B, Raimbault P, Cosson RP, Decottignies P, Martin-Jézéquel V (2015) Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings. J Exp Mar Biol Ecol 469:83–92

    Article  CAS  Google Scholar 

  • Jesus B, Brotas V, Ribeiro L, Mendes CR, Cartaxana P, Paterson DM (2009) Adaptations of microphytobenthos assemblages to sediment type and tidal position. Cont Shelf Res 29:1624–1634

    Article  Google Scholar 

  • Jiang YL, Yoshida T, Quigg A (2012) Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiol Biochem 54:70–77

    Article  CAS  Google Scholar 

  • Jorgensen NOG, Mopper K, Lindroth P (1980) Occurrence, origine and assimilation of free amino acids in an estuarine environment. Ophelia 1:179–192

    Google Scholar 

  • Jorgensen NOG, Lindroth P, Mopper K (1981) Extraction and distribution of free amino acids and ammonium in sediment interstitial waters from the Limfjord, Denmark. Oceanol Acta 4:465–474

    Google Scholar 

  • Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665

    Article  CAS  Google Scholar 

  • Koroleff F (1970) Direct determination of ammonia in natural waters as indophenol blue, information on techniques and methods for seawater analysis. In: International council for the exploration of the sea, pp 19–22

  • Kulk G, van de Poll WH, Visser RJW, Buma AGJ (2013) Low nutrient availability reduces high-irradiance-induced viability loss in oceanic phytoplankton. Limnol Oceanogr 58:1747–1760

    Article  CAS  Google Scholar 

  • Labrenz M, Collins MD, Lawson PA, Tindall BJ, Braker G, Hirsch P (1998) Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. Int J Syst Bacteriol 48:1363–1372

    Article  CAS  Google Scholar 

  • Laroche J, Geider RJ, Graziano LM, Murray H, Lewis K (1993) Induction of specific proteins in eukaryotic algae grown under iron-deficient, phosphorus-deficient, or nitrogen-deficient conditions. J Phycol 29:767–777

    Article  CAS  Google Scholar 

  • Linares F (2006) Effect of dissolved free amino acids (DFAA) on the biomass and production of microphytobenthic communities. J Exp Mar Biol Ecol 330:469–481

    Article  CAS  Google Scholar 

  • Linares F, Sundback K (2006) Uptake of dissolved free amino acids (DFAA) by microphytobenthic communities. Aquat Microb Ecol 42:175–186

    Article  Google Scholar 

  • Lomas MW (2004) Nitrate reductase and urease enzyme activity in the marine diatom Thalassiosira weissflogii (Bacillariophyceae): interactions among nitrogen substrates. Mar Biol 144:37–44

    Article  CAS  Google Scholar 

  • Lomstein BA, Jensen AGU, Hansen JW, Andreasen JB, Hansen LS, Berntsen J, Kunzendorf H (1998) Budgets of sediment nitrogen and carbon cycling in the shallow water of Knebel Vig, Denmark. Aquat Microb Ecol 14:69–80

    Article  Google Scholar 

  • Lu M, Stephens GC (1984) Demonstration of net influx of free amino acids in Pheodactylum tricornutum using high performance liquid chromatography. J Phycol 20:584–589

    Article  CAS  Google Scholar 

  • MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “Secret Garden” of unvegetated, shallow-water marine habitats, 1. Distribution, abondance and primary production. Estuaries 19:186–201

    Article  Google Scholar 

  • Mantoura RFC, Llewellyn CA (1983) The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reversephase high-performance liquid chromatography. Anal Chim Acta 151:297–314

    Article  CAS  Google Scholar 

  • Martin-Jézéquel V, Calu G, Candela L, Amzil Z, Jauffrais T, Séchet V, Weigel P (2015) Effects of organic and inorganic nitrogen on the growth and production of domoic acid by Pseudo-nitzschia multiseries and P. australis (Bacillariophyceae) in culture. Mar Drugs 13:7055–7079

    Article  Google Scholar 

  • McGlathery K, Sundbäck K, Anderson I (2004) The importance of primary producers for benthic nitrogen and phosphorus cycling. In: Nielsen S, Banta G, Pedersen M (eds) Estuarine nutrient cycling: the influence of primary producers. Springer, Amsterdam, pp 231–261

    Chapter  Google Scholar 

  • Meleder V, Barille L, Launeau P, Carrere V, Rince Y (2003) Spectrometric constraint in analysis of benthic diatom biomass using monospecific cultures. Remote Sens Environ 88:386–400

    Article  Google Scholar 

  • Meleder V, Rince Y, Barille L, Gaudin P, Rosa P (2007) Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf bay, France). J Phycol 43:1177–1190

    Article  Google Scholar 

  • Mulvenna PF, Savidge G (1992) A modified manual method for the determination of urea in sea water using diacetylmonoxime reagent. Estuar Coast Shelf Sci 34:429–438

    Article  CAS  Google Scholar 

  • Napoleon C, Raimbault V, Claquin P (2013) Influence of nutrient stress on the relationships between PAM measurements and carbon incorporation in four phytoplankton species. PLoS One 8:e66423. doi:10.1371/journal.pone.0066423

    Article  CAS  Google Scholar 

  • Neilson AH, Larsson T (1980) The utilization of organic nitrogen for growth of algae: physiological aspects. Physiol Plant 48:542–553

    Article  CAS  Google Scholar 

  • Nilsson C, Sundback K (1996) Amino acid uptake in natural microphytobenthic assemblages studied by Microautoradiography. Hydrobiol 332:119–129

    Article  CAS  Google Scholar 

  • North BB, Stephens GC (1972) Amino acid transport in Nitzschia ovalis Arnott. J Phycol 8:64–68

    CAS  Google Scholar 

  • Oaks A (1994) Efficiency of nitrogen utilization in C3 and C4 cereals. Plant Physiol 106:407–414

    CAS  Google Scholar 

  • Oxborough K, Hanlon ARM, Underwood GJC, Baker NR (2000) In vivo estimation of the photosystem II photochemical efficiency of individual microphytobnthic cells using high-resolution imaging of chlorophyll a fluorescence. Limnol Oceanogr 45:1420–1425

    Article  Google Scholar 

  • Parker MS, Armbrust EV (2005) Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 41:1142–1153

    Article  CAS  Google Scholar 

  • Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529

    Article  Google Scholar 

  • Peers GS, Milligan AJ, Harrison PJ (2000) Assay optimization and regulation of urease activity in two marine diatoms. J Phycol 36:523–528

    Article  CAS  Google Scholar 

  • Poulet SA, Martin-Jézéquel V, Delmas D (1985) Gradient of dissolved free amino acids and phytoplankton in a shallow bay. Hydrobiol 121:11–17

    Article  CAS  Google Scholar 

  • Qi HJ, Wang JT, Wang ZY (2013a) A comparative study of maximal quantum yield of photosystem II to determine nitrogen and phosphorus limitation on two marine algae. J Sea Res 80:1–11

    Article  Google Scholar 

  • Qi HJ, Wang JT, Wang ZY (2013b) A comparative study of the sensitivity of F (v)/F (m) to phosphorus limitation on four marine algae. J Ocean Univ Chin 12:77–84

    Article  CAS  Google Scholar 

  • Raimbault P, Pouvesle W, Diaz F, Garcia N, Sempere R (1999) Wet-oxidation and automated colorimetry for simultaneous determination of organic carbon, nitrogen and phosphorus dissolved in seawater. Mar Chem 66:161–169

    Article  CAS  Google Scholar 

  • Rao VNR, Sridharan VT (1980) Uptake of nitrate, ammonium and nitrite by Pleurosigma aestuarii (Breb.) Wm. Sm., an estuarine diatom. Seaweed Res Utiln 4:25–30

    CAS  Google Scholar 

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221

    CAS  Google Scholar 

  • Ribeiro L, Brotas V, Mascarell G, Coute A (2003) Taxonomic survey of the microphytobenthic communities of two Tagus estuary mudflats. Acta Oecol Int J Ecol 24:117–123

    Article  Google Scholar 

  • Roy S (1988) Effects of changes in physiological conditions on HPLC-defined chloropigment composition of Phaeodactylum tricornutum (Bohlin) in batch and turbidostat cultures. J Exp Mar Biol Ecol 118:137–149

    Article  CAS  Google Scholar 

  • Sarthou G, Timmermans KR, Blain S, Tréguer P (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42

    Article  CAS  Google Scholar 

  • Scholz B, Liebezeit G (2013) Biochemical characterisation and fatty acid profiles of 25 benthic marine diatoms isolated from the Solthorn tidal flat (Southern North Sea). Appl Phycol 25:453–465

    Article  CAS  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non- intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70

    Google Scholar 

  • Smil V (2000) Phosphorus in the environment: natural flows and human interferences. Annu Rev Energy Env 25:53–88

    Article  Google Scholar 

  • Stephens GC (1981) The trophic role of dissolved organic material. In: Longhurst AR (ed) Analysis of marine ecosystems. Academic, London, pp 271–292

    Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of sea water analysis. Bull Fish Res Board Can 167:1–311

    Google Scholar 

  • Sundback K, Miles A, Goransson E (2000) Nitrogen fluxes denitrification and the role of microphytobenthos in microtidal shallow-water sediments: an annual study. Mar Ecol Prog Ser 200:59–76

    Article  CAS  Google Scholar 

  • Sundback K, Linares F, Larson F, Wulff A, Engelsen A (2004) Benthic nitrogen fluxes along a depth gradient in a microtidal fjord: the role of denitrification and microphytobenthos. Limnol Oceanogr 49:1095–1107

    Article  Google Scholar 

  • Sundback K, Lindehoff E, Graneli E (2011) Dissolved organic nitrogen: an important source of nitrogen for the microphytobenthos in sandy sediment. Aquat Microb Ecol 63:89–100

    Article  Google Scholar 

  • Syrett PJ (1981) Nitrogen metabolism in microalgae. In: Platt T (ed) Physiological bases of phytoplankton ecology. Can Bull Fish Aquat Sci 210:182–210

  • Syrett PJ, Flynn KJ, Molloy CJ, Dixon GK, Peplinska AM, Cresswell RC (1986) Effects of nitrogen deprivation on rates of uptake of nitrogenous compounds by the diatom, Pheodactylum tricornutum Bohlin. New Phytol 102:39–44

    Article  CAS  Google Scholar 

  • Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20

    Article  CAS  Google Scholar 

  • Underwood GJC, Kromkamp J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. In: Nedwell DB, Raffaelli DG (Eds) Adv Ecol Res. Academic, pp. 93–153

  • Van Leeuwe MA, Brotas V, Consalvey M, Forster RM, Gillespie D, Jesus B, Roggeveld J, Gieskes WWC (2008) Photoacclimation in microphytobenthos and the role of xanthophyll pigments. Eur J Phycol 43:123–132

    Article  CAS  Google Scholar 

  • Vincent WF (1992) The daily pattern of nitrogen uptake by phytoplankton in dynamic mixed layer environments. In: Berman T, Gons HJ, Mur LR (eds) The daily growth cycle of phytoplankton. Hydrobiol 238:37–52

  • Waser NAD, Harrison PJ, Nielsen B, Calvert SE (1998) Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnol Oceanogr 43:215–224

    Article  CAS  Google Scholar 

  • Wheeler PA, North BB, Stephens GC (1974) Amino acid uptake by marine phytoplankter. Limnol Oceanogr 19:249–259

    Article  CAS  Google Scholar 

  • Wheeler PA, Kirchman DL, Landry MR, Kokkinakis SA (1989) Diel periodicity in ammonium uptake and regeneration in the oceanic subarctic Pacific: implications for interactions in microbial food webs. Limnol Oceanogr 34:1025–1033

    Article  CAS  Google Scholar 

  • White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682

    Article  CAS  Google Scholar 

  • Wolfstein K, Stal LJ (2002) Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar Ecol Prog Ser 236:13–22

    Article  Google Scholar 

Download references

Acknowledgments

This study was part of the COSELMAR project carried out with the support of the “Region Pays de la Loire”, the “MSH Ange Guépin”, the Research Federation CNRS 3473 “Institut Universitaire Mer et Littoral” and the University of Nantes. The author would also like to Denis Loquet from the CEISAM for the elemental analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thierry Jauffrais.

Additional information

Responsible Editor: K. Bischof.

Reviewed by Undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jauffrais, T., Jesus, B., Méléder, V. et al. Physiological and photophysiological responses of the benthic diatom Entomoneis paludosa (Bacillariophyceae) to dissolved inorganic and organic nitrogen in culture. Mar Biol 163, 115 (2016). https://doi.org/10.1007/s00227-016-2888-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2888-9

Keywords

Navigation