Abstract
The heterotrophic utilization of organic substrates by diatoms is likely an important survival strategy when light levels are too low for photosynthesis. The objectives of this study were: (1) to determine if heterotrophic utilization of a large array of organic compounds by eight common freshwater benthic diatom taxa was light-dependent, and (2) to determine if organic substrate utilization patterns differed between dark-grown diatoms and bacteria as a possible means of reducing competition by niche separation. Eight light- and dark-grown diatom taxa and five bacterial species were incubated in 96-well Biolog® Microtiter plates with each well containing 1 of 95 different organic substrates. Oxidation rates of each organic substrate were measured through time. There was a substantial increase in the number of organic substrates oxidized by diatoms grown in the dark compared to their light-grown counterparts, indicating that the transport systems for these molecules may be light activated. Therefore, diatoms likely only utilize these metabolically expensive uptake mechanisms when they are necessary for survival, or when substrates are plentiful. A principal components analysis indicated discernible differences in the types of organic-C substrates utilized by dark-grown diatoms and bacteria. Although bacteria were able to oxidize a more diverse array of organic substrates including carboxylic acids and large polymers, diatoms appeared to more readily utilize the complex carbohydrates. By oxidizing different organic substrates than bacteria, heterotrophically metabolizing diatoms may be reducing direct competition and enhancing coexistence with bacteria.
Similar content being viewed by others
References
R. K. Allison H. E. Skipper M. R. Reid W. A. Short G. L. Hogan (1953) ArticleTitleStudies on the photosynthetic reaction I. The assimilation of acetate by Nostoc muscorum Journal of Biological Chemistry 204 197–205 Occurrence Handle1:CAS:528:DyaG3sXntlGmuw%3D%3D Occurrence Handle13084591
C. Amblard (1991) ArticleTitleCarbon heterotrophic activity of microalgae and cyanobacteria – ecological significance Annee Biologique 30 6–107
N. J. Anitia J. Y. Cheng F. J. R. Taylor (1969) ArticleTitleThe heterotrophic growth of a marine photosynthetic cryptomonad (Chroomonas saline) Proceedings of the International Seaweed Symposium 6 17–29
J Bertrand (1992) ArticleTitleMouvements des diatomees II -synthese des mouvements Cryptogamie: Algologie 13 49–71
J. M. Burkholder R. G. Wetzel K. L. Klomparens (1990) ArticleTitleDirect comparison of phosphate uptake by adnate and loosely attached microalgae within an intact biofilm matrix Applied Environmental Microbiology 56 2882–2890 Occurrence Handle1:CAS:528:DyaK3cXls1yktrc%3D
J. J. Cole (1982) ArticleTitleInteractions between bacteria and algae in aquatic ecosystems Annual Review of Ecology and Systematics 13 291–314 Occurrence Handle10.1146/annurev.es.13.110182.001451
H. J. Lange ParticleDe D. P. Morris C. E. Williamson (2003) ArticleTitleSolar ultraviolet photodegradation of DOC may stimulate freshwater food webs Journal of Plankton Research 25 111–117
J. P. Descy B. Leporcq L. Viroux C. Francois P. Servais (2002) ArticleTitlePhytoplankton production, exudation, and bacterial reassimilation in the River Meuse (Belgium) Journal of Plankton Research 24 161–166 Occurrence Handle10.1093/plankt/24.3.161
W. K. Dodds (1992) ArticleTitleA modified fiber-optic light microprobe to measure spherically integrated photosynthetic photon flux density: Characteristics of periphyton photosynthesis-irradiance patterns Limnology and Oceanography 37 871–878 Occurrence Handle1:CAS:528:DyaK3sXktVSk
K. J. Flynn T. Butler (1986) ArticleTitleNitrogen sources for growth of marine microalgae: Role of dissolved free amino acids Marine Ecology Progress Series 34 281–304 Occurrence Handle1:CAS:528:DyaL2sXhtlCku7g%3D
H. Gurbuz E. Kivrak (2003) ArticleTitleSeasonal variations of benthic algae of Kuzgun Dam Reservoir and their relationship to environmental factors Fresenius Environmental Bulleting 12 1025–1032 Occurrence Handle1:CAS:528:DC%2BD3sXotlGmsLo%3D
J. A. Hellebust (1971) ArticleTitleGlucose uptake by Cyclotella cryptica: Dark induction and light inactivation of transport system Journal of Phycology 7 345–349
J. A. Hellebust J. Lewin (1977) Heterotrophic nutrition Werner (Eds) The Biology of Diatoms University of California Press Berkeley 169–197
C. Hudon E. Bourget (1981) ArticleTitleInitial colonization of artificial substrate: community development and structure studied by scanning electron microscopy Canadian Journal of Fisheries and Aquatic Sciences 38 1371–1384
R. E. Johnson N. C. Tuchman C. G. Peterson (1997) ArticleTitleChanges in the vertical microdistribution of diatoms within a developing periphyton mat Journal of the North American Benthological Society 16 503–519
B. B. Jorgenson N. P. Revsbech Y. Cohen (1983) ArticleTitlePhotosynthesis and structure of benthic microbial mats: Microelectrode and SEM studies of four cyanobacterial communities Limnology and Oceanography 28 1075–1093
J. L. Klug (2005) ArticleTitleBacterial response to dissolved organic matter affects resource availability for algae Canadian Journal of Fisheries and Aquatic Sciences 62 472–481 Occurrence Handle10.1139/f04-229 Occurrence Handle1:CAS:528:DC%2BD2MXkvFCisLw%3D
S. K. Liehr M. T. Suidan J. W. Eheart (1990) ArticleTitleA modeling study of carbon and light limitation in algal biofilms Biotechnology and Bioengineering 35 233–243 Occurrence Handle10.1002/bit.260350304 Occurrence Handle1:CAS:528:DyaK3cXhtFOgsL4%3D
M. S. Liu J. A. Hellebust (1973) ArticleTitleUtilization of amino acids as nitrogen sources, and their effects on nitrate reductase in the marine diatom Cyclotella cryptica Canadian Journal of Microbiology 20 1119–1124
P. V. McCormick R. J. Stevenson (1991) ArticleTitleMechanisms of benthic algal succession in lotic environments Ecology 72 1835–1848
A. Michels (1998) ArticleTitleEffects of sewage water on diatoms (Bacillariophyceae) and water quality in two tropical streams in Costa Rica Revista de Biología Tropical 46 153–175
A. H. Neilson R. A. Lewin (1974) ArticleTitleThe uptake and utilization of organic carbon by algae; an essay in comparative biochemistry Phycologia 13 227–264 Occurrence Handle1:CAS:528:DyaE2MXkslGhu7c%3D
C. Nilsson K. Sundbäck (1996) ArticleTitleAmino acid uptake in natural microphytobenthic assemblages studied by microautoradiography Hydrobiologia 332 119–129 Occurrence Handle10.1007/BF00016691 Occurrence Handle1:CAS:528:DyaK28XnsV2kur4%3D
H. W. Paerl (1991) ArticleTitleEcophysiological and trophic implications of light-stimulated amino acid utilization in marine picoplankton Applied Environmental Microbiology 57 473–479 Occurrence Handle1:CAS:528:DyaK3MXhtFyhtbc%3D
A. C. Palmisano J. B. SooHoo D. C. White G. A. Smith G. R. Staton L. H. Burckle (1985) ArticleTitleShade adapted benthic diatoms beneath Antarctica sea ice Journal of Phycology 21 664–667
B. C. Parker H. C. Bold T. R. Deason (1961) ArticleTitleFacultative heterotrophy in some chlorococcacean algae Science 133 761–763
M. J. Pelczar R. Reid E. C. S. Chan (1977) Microbiology McGraw-Hill Book Company New York 952
M. Petit G. P. Alves P. Lavandier (1999) ArticleTitlePhytoplankton exudation, bacterial reassimilation and production for three diel cycles in different trophic conditions Archiv für Hydrobiologie 146 285–309 Occurrence Handle1:CAS:528:DC%2BD3cXks1Cn
A. Puddu A. Zoppini S. Fazi M. Rosati S. Amalfitano E. Magaletti (2003) ArticleTitleBacterial uptake of DOM released from P-limited phytoplankton FEMS Microbial Ecology 46 257–268 Occurrence Handle1:CAS:528:DC%2BD3sXptlOru7g%3D
R. B. Rivkin M. Putt (1987) ArticleTitleHeterotrophy and photoheterotrophy by Antarctic microalgae: Light-dependent incorporation of amino acids and glucose Journal of Phycology 23 442–452 Occurrence Handle1:CAS:528:DyaL2sXmtlegsL4%3D
M. A. Schollett (1998) Organic nutrient preferences for benthic diatoms: An approach to quantifying heterotrophic metabolism Loyola University Chicago Chicago, IL 91
R. L. Sinsabaugh A. E. Linkins (1988) ArticleTitleExoenzyme activity associated with lotic epilithon Freshwater Biology 20 249–261 Occurrence Handle1:CAS:528:DyaK3cXkt1yrtrc%3D
E. J. Stadelmann (1962) Permeability Lewin (Eds) Physiology and Biochemistry of Algae Academic Press New York 493–528
A. D. Steinman C. D. McIntire S. V. Gregory G. A. Lamberti L. R. Ashkenas (1987) ArticleTitleEffects of herbivore type and density on taxonomic structure and physiognomy of algal assemblages in laboratory streams Journal of the North American Benthological Society 6 175–188
W. D. P. Stewart (1974) Algal Physiology and Biochemistry University of California Press Los Angeles 989
N. C. Tuchman (1996) The role of heterotrophy in benthic algae R. J. Stevenson M. Bothwell R. Lowe (Eds) Algal Ecology: Freshwater Benthic Habitats Academic Press San Diego 299–319
N. C. Tuchman R. J. Stevenson (1991) ArticleTitleEffects of selective grazing by snails on benthic algal succession Journal of the North American Benthological Society 10 430–443
N. Wasmund (1987) ArticleTitleLive algae in deep sediment layers Internationale Revue der Gesamten Hydrobiologie 74 589–597
R. G. Wetzel P. G. Hatcher T. S. Bianchi (1995) ArticleTitleNatural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism Limnology and Oceanography 40 1369–1380 Occurrence Handle1:CAS:528:DyaK28XpvVOlsA%3D%3D
Q. Zhang R. Gradinger Q. S. Zhou (2003) ArticleTitleCompetition within the marine microalgae over the polar dark period in the Greenland Sea of high Arctic Acta Oceanologica Sinica 22 233–242
T. Zotina O. Koster F. Juttner (2003) ArticleTitlePhotoheterotrophy and light-dependent uptake of organic and organic nitrogenous compounds by Planktothrix rubescens under low irradiance Freshwater Biology 48 1859–1872 Occurrence Handle10.1046/j.1365-2427.2003.01134.x Occurrence Handle1:CAS:528:DC%2BD3sXovFWgsrc%3D
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tuchman, N.C., Schollett, M.A., Rier, S.T. et al. Differential Heterotrophic Utilization of Organic Compounds by Diatoms and Bacteria under Light and Dark Conditions. Hydrobiologia 561, 167–177 (2006). https://doi.org/10.1007/s10750-005-1612-4
Issue Date:
DOI: https://doi.org/10.1007/s10750-005-1612-4