Microbial Food Webs in Aquatic and Terrestrial Ecosystems

  • Behzad MostajirEmail author
  • Christian AmblardEmail author
  • Evelyne Buffan-Dubau
  • Rutger De Wit
  • Robert Lensi
  • Télesphore Sime-Ngando


In microbial food webs, different types of interactions occur between microorganisms themselves and with meio- and macroorganisms. After an historical and general introduction, the biological components of the microbial food webs in the pelagic and benthic marine and lake ecosystems, as well as in the terrestrial ecosystems, are presented. The functioning of the microbial food webs in different ecosystems is illustrated and explained, including the trophic pathways and transfer of matter from microbial food webs toward meio- and macroorganisms of the superior trophic levels, the nutrient recycling in the aquatic environments, and the decomposition of organic matter in soils. Finally, the factors regulating microbial food webs, primarily “top-down” and “bottom-up” controls, are described with a special focus on the role of viruses in the aquatic microbial food webs.


Biodiversity Biogeochemical cycles Ecological interactions Microbial food webs Microbial loop 


  1. Ackermann H-W (2003) Bacteriophage observations and evolution. Res Microbiol 154:245–251PubMedCrossRefGoogle Scholar
  2. Aller RC, Aller JY (1992) Meiofauna and solute transport in marine muds. Limnol Oceanogr 37:1018–1033CrossRefGoogle Scholar
  3. Amblard C, Carrias JF, Bourdier G, Maurin N (1995) The microbial loop in a humic lake: seasonal and vertical variations in the structure of the different communities. Hydrobiologia 300(301):71–84CrossRefGoogle Scholar
  4. Amblard C, Boisson JC, Bourdier G, Fontvieille D, Gayte X, Sime-Ngando T (1998) Ecologie microbienne en milieu aquatique: des virus aux protozoaires. Rev Sc. Eau, N° Spécial: Les Sciences de l’Eau: Bilan et perspectives, 145–162Google Scholar
  5. Anderson JM (2000) Food web functioning and ecosystem processes. In: Colemab DC, Hendrix PF (eds) Invertebrates as webmasters in ecosystems. CABI Publishing, Wallunford, pp 3–24CrossRefGoogle Scholar
  6. Angly FE et al (2006) The marine viromes of four oceanic regions. PLoS Biol 4:e368PubMedCentralPubMedCrossRefGoogle Scholar
  7. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  8. Badejo MA, Tian G (1999) Abundance of soil mites under four agroforestry tree species with contrasting litter quality. Biol Fertil Soils 30:107–112CrossRefGoogle Scholar
  9. Bardgett RD (2005a) Organism interactions and soil processes. In: Crawley MJ, Little C, Southwood TRE, Ulfstrand S (eds) The biology of soil, a community and ecosystem approach. Oxford University Press, Oxford, UK, pp 57–85Google Scholar
  10. Bardgett RD (2005b) The diversity of life in soil. In: Crawley MJ, Little C, Southwood TRE, Ulfstrand S (eds) The biology of soil, a community and ecosystem approach. Oxford University Press, Oxford, UK, pp 24–56Google Scholar
  11. Beare MH, Coleman DC, Crossley DA, Hendrix PF, Odum EP (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant and Soil 170:5–22CrossRefGoogle Scholar
  12. Bec A, Martin-Creuzburg D, von Elert E (2006) Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnol Oceanogr 51:1699–1707CrossRefGoogle Scholar
  13. Bergh O, Børsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468PubMedCrossRefGoogle Scholar
  14. Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284PubMedCrossRefGoogle Scholar
  15. Brown GG (1995) How do earthworms affect microfloral and faunal community diversity. Plant and Soil 170:209–231CrossRefGoogle Scholar
  16. Buffan-Dubau E, Carman KR (2000) Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnol Oceanogr 45:381–395CrossRefGoogle Scholar
  17. Carpenter SR (1988) Complex interactions in lake communities. Springer, New YorkCrossRefGoogle Scholar
  18. Carrias JF, Amblard C, Bourdier G (1998) Seasonal dynamics and vertical distribution of planktonic ciliates and their relationship to microbial food resources in the oligomesotrophic lake Pavin. Arch Hydrobiol 143:227–255Google Scholar
  19. Colombet J (2008) Importance de la variabilité verticale dans un lac méromictique profond: diversité et activité lysogène des communautés virales. Thèse de Doctorat, Université Blaise Pascal, 204 pGoogle Scholar
  20. Curtis TP, Sloan WT, Scannel JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci U S A 99:10494–10499PubMedCentralPubMedCrossRefGoogle Scholar
  21. Cushing DH (1989) A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J Plank Res 11:1–13CrossRefGoogle Scholar
  22. De Ruiter PC, Neutel AN, Moore JC (1995) Energetics, patterns of interactions strengths and stability in real ecosystems. Science 269:1257–1260PubMedCrossRefGoogle Scholar
  23. De Ruiter PC, Neutel AN, Moore JC (1997) Soil foodweb interactions and modelling. In: Benckiser G (ed) Fauna in soil ecosystems. Dekker, New York, pp 363–386Google Scholar
  24. Degens B, Harris JA (2000) Decreases in organic C reserves in soil can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196CrossRefGoogle Scholar
  25. Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689PubMedCentralPubMedCrossRefGoogle Scholar
  26. Dolan JR (1997) Phosphorus and ammonia excretion by planktonic protists. Mar Geol 139:109–122CrossRefGoogle Scholar
  27. Edwards RA, Rohwer F (2005) Viral metagenomics. Nat Rev Microbiol 3:504–510PubMedCrossRefGoogle Scholar
  28. Egerton-Warburton L, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496CrossRefGoogle Scholar
  29. Filippini M, Buesing N, Bettarel Y, Sime-Ngando T, Gessner MO (2006) Infection paradox: high abundance but low impact of freshwater benthic viruses. Appl Environ Microbiol 72:4893–4898PubMedCentralPubMedCrossRefGoogle Scholar
  30. Foissner W (1997a) Global soil ciliate (Protozoa: Ciliophora) diversity: a probability-based approach using large sample collections from Africa, Australia and Antarctica. Biodivers Conserv 5:1627–1638CrossRefGoogle Scholar
  31. Foissner W (1997b) Soil ciliates (Protozoa: Ciliophora) from evergreen rain forest of Australia, South America and Costa Rica: diversity and description of new species. Biol Fertil Soils 25:317–339CrossRefGoogle Scholar
  32. Forterre P (2007) Microbes de l’enfer. Edition Belin, ParisGoogle Scholar
  33. Fouilland E, Mostajir B (2010) Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwater, transitional, coastal and oceanic waters. FEMS Microbiol Ecol 73:419–429PubMedCrossRefGoogle Scholar
  34. 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 78:206–209CrossRefGoogle Scholar
  35. 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 29:369–376CrossRefGoogle Scholar
  36. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548PubMedCrossRefGoogle Scholar
  37. Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, Berlin/HeidelbergGoogle Scholar
  38. Grami B, Rasconi S, Niquil N, Jobard M, Saint-Béat B, Sime-Ngando T (2011) Functional effects of parasites on food web properties during the spring diatom bloom in Lake Pavin: a linear inverse modeling analysis. PLoS One 6:e23273PubMedCentralPubMedCrossRefGoogle Scholar
  39. Hedlund K, Boddy L, Preston CM (1991) Mycelial response of the soil fungus, Mortierella Isabellina, to grazing by Onychiurus armatus (collembolan). Soil Biol Biochem 23:361–366CrossRefGoogle Scholar
  40. Hobbie JE, Daley RJ, Jasper S (1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228PubMedCentralPubMedGoogle Scholar
  41. Jardillier L, Boucher D, Personnic S, Jacquet S, Thenot A, Sargos D, Amblard C, Debroas D (2005) Relative importance of nutrients and mortality factors on prokaryotic community composition in two lakes of different trophic status: microcosm experiments. FEMS Microbiol Ecol 53:429–443PubMedCrossRefGoogle Scholar
  42. Kagami M, De Bruin A, Ibelings BW, Van Donk E (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578:113–129CrossRefGoogle Scholar
  43. Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179PubMedCrossRefGoogle Scholar
  44. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D (2003) A giant virus in amoebae. Science 299:2033PubMedCrossRefGoogle Scholar
  45. Laval-Peuto M, Heinbokel JF, Anderson R, Rassoulzadegan F, Sherr BF (1986) Role of micro- and nanozooplankton in marine food webs. Insect Sci Appl 7:387–395Google Scholar
  46. Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15CrossRefGoogle Scholar
  47. Lawrence JR, Scharf B, Packroff G, Neu TR (2002) Microscale evaluation of the effects of grazing by invertebrates with contrasting feeding modes on river biofilm architecture and composition. Microb Ecol 43:199–207CrossRefGoogle Scholar
  48. Lefèvre E, Bardot C, Noël C, Carrias J-F, Viscogliosi E, Amblard C, Sime-Ngando T (2007) Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol 9:61–71PubMedCrossRefGoogle Scholar
  49. Legendre L, Rassoulzadegan F (1995) Plankton and nutrient dynamics in marine waters. Ophelia 41:153–172CrossRefGoogle Scholar
  50. Li KW, Subba Rao DV, Harrison GW, Smith CJ, Cullen JJ, Irwin B, Platt T (1983) Autotrophic picoplankton in the tropical ocean. Science 219:292–295PubMedCrossRefGoogle Scholar
  51. Liess A, Hillebrand H (2004) Direct and indirect effects in herbivore–periphyton interactions. Arch Hydrobiol 159:433–453CrossRefGoogle Scholar
  52. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW (2005) Photosynthetic genes in marine viruses yield proteins during host infection. Nature 438:86–89PubMedCrossRefGoogle Scholar
  53. Majdi N, Mialet B, Boyer S, Tackx M, Leflaive J, Boulêtreau S, Ten-Hage L, Julien F, Fernandez R, Buffan-Dubau E (2012a) The relationship between epilithic biofilm stability and its associated meiofauna under two patterns of flood disturbance. Fresh Sci 31:38–50CrossRefGoogle Scholar
  54. Majdi N, Tackx M, Buffan-Dubau E (2012b) Trophic positioning and microphytobenthic carbon uptake of biofilm-dwelling meiofauna in a temperate river. Fresh Biol 57:1180–1190CrossRefGoogle Scholar
  55. Mann NH (2003) Phages of the marine cyanobacterial phytoplankton. FEMS Microbiol Rev 27:17–34PubMedCrossRefGoogle Scholar
  56. Maranger R, Bird DE (1996) High concentrations of viruses in the sediments of Lac Gilbert, Quebec. Microb Ecol 31:141–151PubMedGoogle Scholar
  57. Mathieu M, Leflaive J, Ten-Hage L, de Wit R, Buffan-Dubau E (2007) Free-living nematodes affect oxygen turn-over of artificial diatom biofilms. Aquat Microb Ecol 49:281–291CrossRefGoogle Scholar
  58. McLean MA, Parkinson D (2000) Field evidence of the effects of the epigenic earthworm Dendrobaena octaedra on the microfungal community in pine forest floor. Soil Biol Biochem 32:351–360CrossRefGoogle Scholar
  59. McQueen DJ, Johannes MRS, Post JR, Steward TJ, Lean DRS (1989) Bottom-up and top-down impacts on freshwater pelagic community structure. Ecol Monogr 59:289–310CrossRefGoogle Scholar
  60. Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR (2000) The fate of intertidal microphytobenthos carbon: an in situ 13C labelling study. Limnol Oceanogr 45:1224–1234CrossRefGoogle Scholar
  61. Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB (2001) What is the observed relationship between species richness and productivity? Ecology 82:2381–2396CrossRefGoogle Scholar
  62. Moens T, Traunspurger W, Bergtold M (2006) Feeding ecology of free-living benthic nematodes. In: Abebe E, Traunspurger W, Andrassy I (eds) Freshwater nematodes: ecology and taxonomy. CABI Publishing, Wallingford, pp 105–131CrossRefGoogle Scholar
  63. Moody SA, Piearce TG, Dighton J (1996) Fates of some fungal spores associated with wheat straw decomposition on passage through the guts of Lumbricus terrestris and Aporrectodea longa. Soil Biol Biochem 28:533–537CrossRefGoogle Scholar
  64. Moran XA, Alonso-Saez L (2011) Independence of bacteria on phytoplankton? Insufficient support for Fouilland and Mostajir’s (2010) suggested new concept. FEMS Microbiol Ecol 78:203–205PubMedCrossRefGoogle Scholar
  65. Pischedda L, Cuny P, Esteves JL, Poggiale J-C, Gilbert F (2012) Spatial oxygen heterogeneity in a Hediste diversicolor irrigated burrow. Hydrobiologia 680:109–124CrossRefGoogle Scholar
  66. Pomeroy LR (1974) The ocean’s food web, a changing paradigm. BioSci 24:499–504CrossRefGoogle Scholar
  67. Pomeroy LR (1991) Status and future needs in protozoan ecology. In: Reid PC, Turley CM, Burkill PH (eds) Protozoa and their role in marine processes. Nato Asi series. Springer, New York, pp 475–492CrossRefGoogle Scholar
  68. Renault P, Stengel P (1994) Modelling oxygen diffusion in aggregated soils: anaerobiosis inside the aggregates. Soil Sci Soc Am J 58:1017–1023CrossRefGoogle Scholar
  69. Riemann F, Helmke E (2002) Symbiotic relations of sediment agglutinating nematodes and bacteria in detrital habitats: the enzyme-sharing concept. PSZN I Mar Ecol 23:93–113CrossRefGoogle Scholar
  70. Rohwer F, Thurber RV (2009) Viruses manipulate the marine environment. Nature 459:207–212PubMedCrossRefGoogle Scholar
  71. Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99–108PubMedCrossRefGoogle Scholar
  72. Schmidt O, Curry JP, Dyckmans J, Rota E, Scrimgeour CM (2004) Dual stable isotope analysis (delta C-13 and delta N-15) of soil invertebrates and their food source. Pedobiologia 48:171–180CrossRefGoogle Scholar
  73. Schulz HN, Jorgensen BB (2001) Big bacteria. Annu Rev Microbiol 55:105–137PubMedCrossRefGoogle Scholar
  74. Sextone AJ, Revbesh NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651CrossRefGoogle Scholar
  75. Sherr EB, Sherr BF (1988) Role of microbes in pelagic food webs: a revised concept. Limnol Oceanogr 33:1225–1227CrossRefGoogle Scholar
  76. Sieburth JMCN, Smetacek V, Lenz J (1978) Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol Oceanogr 23:1256–1263CrossRefGoogle Scholar
  77. Sime-Ngando T (1997) Importance des virus dans la structure et le fonctionnement des réseaux trophiques microbiens aquatiques. Ann Biol 36:181–210Google Scholar
  78. Sime-Ngando T (2012) Phytoplankton chytridiomycosis: fungal parasites of phytoplankton and their imprints on the food web dynamics. In: Grossart HP, Reimann L, Tang KW (eds) Molecular and functional ecology of aquatic microbial symbionts, vol 3. Frontiers Microbiology, p 361Google Scholar
  79. Sime-Ngando T, Colombet J (2009) Viruses and prophages in aquatic ecosystems. Can J Microbiol 55:95–109PubMedCrossRefGoogle Scholar
  80. Sime-Ngando T, Niquil N (2011) Disregarded microbial diversity and ecological potentials in aquatic systems. Development in hydrobiology, vol 216. Springer, DordrechtGoogle Scholar
  81. Sime-Ngando T, Bettarel Y, Chartogne C, Sean K (2003) The imprint of wild viruses on freshwater microbial ecology. Recent Res Dev Microbiol 7:481–497Google Scholar
  82. Suttle CA (2005) Viruses in the sea. Nature 437:356–361PubMedCrossRefGoogle Scholar
  83. Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev 5:801–812Google Scholar
  84. Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. University of California Press, BerkeleyGoogle Scholar
  85. Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2010) Invertébrés d’eau douce: systématique, biology, écologie. CNRS Éditions, ParisGoogle Scholar
  86. Thingstad TF (2000) Element of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacteria viruses in aquatic systems. Limnol Oceanogr 45:1320–1328CrossRefGoogle Scholar
  87. Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity: magnitude, dynamics and controlling factors. Science 296:1064–1066PubMedCrossRefGoogle Scholar
  88. Verity PG (1991) Feeding in planktonic protozoans – evidence for non-random acquisition of prey. J Protozool 38:69–76CrossRefGoogle Scholar
  89. Wardle DA (2002) Linking the aboveground and belowground components. Princeton University Press, PrincetonGoogle Scholar
  90. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181PubMedCrossRefGoogle Scholar
  91. Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6:1–11PubMedCrossRefGoogle Scholar
  92. Wetzel RG, Rich PH, Miller MC, Allen HL (1972) Metabolism of dissolved and particulate detrital carbon in a temperate hard-water lake. In: Melchiorri-Santolini U, Hopton JW (eds) Detritus and its role in aquatic ecosystems, vol 29. Memoire Inst Ital Idrobiol, pp 185–243Google Scholar
  93. Yeates GW, Bongers T (1999) Nematode biodiversity in agroecosystems. Agric Ecosyst Environ 74:113–135CrossRefGoogle Scholar
  94. Yeates GW, Bongers T, De Groede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera – an outline for ecologists. J Nematol 25:315–331PubMedCentralPubMedGoogle Scholar
  95. Yeates GW, Bardgett RD, Cook R, Hobbs PJ, Bowling PJ, Potter JF (1997) Faunal and microbial diversity in three Welsh grassland soils under conventional and organic managements regimes. J Appl Ecol 34:453–471CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Behzad Mostajir
    • 1
    Email author
  • Christian Amblard
    • 2
    Email author
  • Evelyne Buffan-Dubau
    • 3
  • Rutger De Wit
    • 1
  • Robert Lensi
    • 4
  • Télesphore Sime-Ngando
    • 2
  1. 1.Écologie des systèmes marins côtiers (ECOSYM, UMR5119)Universités Montpellier 2 et 1, CNRS-Ifremer-IRDMontpellier Cedex 05France
  2. 2.Laboratoire Microorganismes: Génome et Environnement (LMGE)UMR CNRS 6023, Université Blaise Pascal, Clermont UniversitéAubère CedexFrance
  3. 3.Laboratoire d’Écologie Fonctionnelle et Environnement (ECOLAB)UMR CNRS 5245, Université Paul SabatierToulouse Cedex 9France
  4. 4.Centre d’Écologie Fonctionnelle et Évolutive (CEFE), Département d’Écologie FonctionnelleUMR 5175Montpellier Cedex 5France

Personalised recommendations