Indirect interactions in the microbial world: Specificities and similarities to plant-insect systems

Population Ecology

Volumn 52, Issue 4, 2010, Pages 475-483

  Miki, Takeshi ^a   Jacquet, Stéphan ^b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b UMR CARRTEL   (France)

Author keywords

Aquatic microbial community; Bacteria; Bacteriophage; Predator parasite links; Trait mediated indirect interactions

Indexed keywords

AQUATIC ECOSYSTEM; BACTERIOPHAGE; BACTERIUM; COMMUNITY STRUCTURE; EXPERIMENTAL STUDY; MICROBIAL COMMUNITY; PLANT-INSECT INTERACTION; PREDATION; PROTOZOAN; TROPHIC INTERACTION;

BACTERIA (MICROORGANISMS); HEXAPODA; PROTOZOA;

EID: 78650311471     PISSN: 14383896     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10144-010-0235-4     Document Type: Article

References (85)

1. Agrawal AA, Gorski PM, Tallamy DW (1999) Polymorphism in plant defense against herbivory: constitutive and induced resistance in Cucumis sativus. J Chem Ecol 25: 2285-2304.
2. 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: 257-263.
3. Bettarel Y, Sime-Ngando T, Amblard C, Carrias JF, Portelli C (2003) Virioplankton and microbial communities in aquatic systems: a seasonal study in two lakes of different trophy. Freshw Biol 48: 810-822.
4. Bettarel Y, Sime-Ngando T, Amblard C, Dolan J (2004) Viral activity in two contrasting lake ecosystems. Appl Environ Microbiol 70: 2941-2951.
5. Bettarel Y, Sime-Ngando T, Bouvy M, Arfi R, Amblard C (2005) Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of French Massif Central. Aquat Microb Ecol 39: 205-209.
6. Binder B (1999) Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquat Microb Ecol 18: 207-215.
7. Bohannan BJM, Lenski RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3: 362-377.
8. Bongiorni L, Magagnini M, Armeni M, Noble R, Danovaro R (2005) Viral production, decay rates, and life strategies along a trophic gradient in the North Adriatic Sea. Appl Environ Microbiol 71: 6644-6650.
9. Bouvier T, del Giorgio PA (2007) Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ Microbiol 9: 287-297.
10. Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar Ecol Prog Ser 83: 273-280.
11. Choo K, Williams PD, Day T (2003) Host mortality, predation and the evolution of parasite virulence. Ecol Lett 6: 310-315.
12. Colombet J, Sime-Ngando T, Cauchie HM, Fonty G, Hoffmann L, Demeure G (2006) Depth-related gradients of viral activity in Lake Pavin. Appl Environ Microbiol 72: 4440-4445.
13. Corno G (2006) Effects of nutrient availability and Ochromonas sp predation on size and composition of a simplified aquatic bacterial community. FEMS Microbiol Ecol 58: 354-363.
14. Corno G, Jürgens K (2006) Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Appl Environ Microbiol 72: 78-86.
15. Demuth J, Neve H, Witzel KP (1993) Direct electron microscopy study on the morphological diversity of bacteriophage populations in Lake Plußsee. Appl Environ Microbiol 59: 3378-3384.
16. Domaizon I, Viboud S, Fontvieille D (2003) Taxon specific and seasonal variations in flagellates grazing on heterotrophic bacteria on the oligotrophic Lake Annecy-importance of mixotrophy. FEMS Microbiol Ecol 46: 317-329.
17. Evans C, Wilson WH (2008) Preferential grazing of Oxyrrhis marina on virus-infected Emiliania huxleyi. Limnol Oceanogr 53: 2035-2040.
18. Faeth SH (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67: 479-494.
19. Fischer UR, Wieltsching C, Kirschner AKT, Velimirov B (2006) Contribution of virus-induced lysis and protozoan grazing to benthic bacterial mortality estimated simultaneously in microcosms. Environ Microbiol 8: 1394-1407.
20. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548.
21. Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40: 1236-1242.
22. Garza DR, Suttle CA (1995) Large double-stranded DNA viruses which cause the lysis of a marine heterotrophic nanflagellate (Bodo sp.) occur in natural marine viral communitites. Aquat Microb Ecol 9: 203-210.
23. Gleason FH, Kagami M, Lefevre E, Sime-Ngando T (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 22: 17-25.
24. Gonzáles JM, Suttle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar Ecol Prog Ser 94: 1-10.
25. Hahn MW, Höfle MG (1999) Flagellate predation on a bacterial model community: interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl Environ Microbiol 65: 4863-4872.
26. Hewson I, O'Neil JM, Fuhrman JA, Dennison WC (2001) Virus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol Oceanogr 46: 1734-1746.
27. Holt RD, Huxel GR (2007) Alternative prey and the dynamics of intraguild predation: theoretical perspectives. Ecology 88: 2706-2712.
28. Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149: 745-764.
29. Horňák K, Masin M, Jezbera J, Bettarel Y, Nedoma J, Sime-Ngando T, Šimek K (2005) Effects of decreased resource availability, protozoan grazing and viral impact on a structure of bacterioplankton assemblage in a canyon-shaped reservoir. FEMS Microbiol Ecol 52: 315-327.
30. Jacquet S, Domaizon I, Personnic S, Duhamel S, Heldal M, Pradeep Ram AS, Sime-Ngando T (2005) Estimates of protozoan and virus-mediated mortality of bacterioplankton in Lake Bourget (France). Freshw Biol 50: 627-645.
31. Jacquet S, Domaizon I, Personnic S, Sime-Ngando T (2007) Do small grazers influence viral-induced bacterial mortality in Lake Bourget? Fundam Appl Limnol 170: 125-132.
32. Jardillier L, Bettarel Y, Richardot M, Bardot C, Amblard C, Sime-Ngando T, Debroas D (2005) Effects of viruses and predators on prokaryotic community composition. Microb Ecol 50: 557-569.
33. Jüergens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81: 413-434.
34. Karban R, Myers JH (1989) Induced plant-responses to herbivory. Annu Rev Ecol Syst 20: 331-348.
35. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9: 485-498.
36. Kondoh M (2008) Building trophic modules into a persistent food web. Proc Nat Acad Sci USA 105: 16631-16635.
37. La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D (2008) The virophage as a unique parasite of the giant mimivirus. Nature 455: 100-105.
38. Lefèvre E, Bardot C, Noel 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: 61-71.
39. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7: 601-613.
40. Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10: 1-44.
41. Lepère C, Domaizon I, Debroas D (2008) Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Appl Environ Microbiol 74: 2940-2949.
42. Lymer D, Lindstrom ES, Vrede K (2008) Variable important of viral-induced bacterial mortality along gradients of trophic status and humic content in lakes. Freshw Biol 53: 1101-1113.
43. Maranger R, Del Giorgio PA, Bird DF (2002) Accumulation ofdamaged bacteria and viruses in lake exposed to solar radiation. Aquat Microb Ecol 28: 213-227.
44. Martin MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4: 467-477.
45. Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79: 192-200.
46. Massana R, del Campo J, Dinter C, Sommaruga R (2007) Crash of a population of the marine heterotrophic flagellate Cafeteria roenbergensis by viral infection. Environ Microbiol 9: 2660-2669.
47. Middelboe M (2000) Bacterial growth rate and marine virus host dynamics. Microb Ecol 40: 114-124.
48. Middelboe M (2008) Microbial disease in the sea: effects of viruses on carbon and nutrient cycling. In: Ostfeld RS, Keesing F, Eviner VT (eds) Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, pp 242-259.
49. Miki T, Jacquet S (2008) Complex interactions in the microbial world: underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat Microb Ecol 51: 195-208.
50. Miki T, Yamamura N (2005) Intraguild predation reduces bacterial species richness and loosens the viral loop in aquatic systems: 'kill the killer of the winner' hypothesis. Aquat Microb Ecol 40: 1-12.
51. Miki T, Nakazawa T, Yokokawa T, Nagata T (2008) Functional consequences of viral impacts on bacterial communities; a food-web model analysis. Freshw Biol 53: 1142-1153.
52. Motegi C, Nagata T (2007) Enhancement of viral production by addition of nitrogen or nitrogen plus carbon in subtropical surface waters of the South Pacific. Aquat Microb Ecol 48: 27-34.
53. Nakamura M, Miyamoto Y, Ohgushi T (2003) Gall initiation enhances the availability of food resources for herbivorous insects. Funct Ecol 17: 851-857.
54. Namba T, Tanabe K, Maeda N (2008) Omnivory and stability of food webs. Ecol Complex 5: 73-85.
55. Noble RT, Fuhrman JA (1997) Virus decay and its causes in coastal waters. Appl Environ Microbiol 63: 77-83.
56. Noble R, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113-118.
57. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36: 81-105.
58. Ohgushi T (2007) Nontrophic, indirect interaction webs of herbivorous insects. In: Ougushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 221-245.
59. Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31: 2231-2242.
60. Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2: 579-589.
61. Pernthaler J, Posch T, Šimek K, Vrba J, Pernthaler A, Glöckner FO, Nübel U, Psenner R, Amann R (2001) Predator-specific enrichment of Actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl Environ Microbiol 67: 2145-2155.
62. Pinheiro MD, Power ME, Butler BJ, Dayeh VR, Slawson R, Lee LE, Lynn DH, Bols NC (2007) Use of Tetrahymena thermophila to study the role of protozoa in inactivation of viruses in water. Appl Environ Microbiol 73: 643-649.
63. Pradeep Ram AS, Sime-Ngando T (2008) Functional responses of prokaryotes and viruses to grazer effects and nutrient additions in freshwater microcosms. The ISME J 2: 498-509.
64. Pradeep Ram AS, Boucher D, Sime-Ngando T, Debroas D, Romagoux JC (2005) Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: coupling with temperature. Microb Ecol 50: 64-72.
65. Šimek K, Pernthaler J, Weinbauer MG, Horňák K, Dolan JR, Nedoma J, Masin M, Amann R (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl Environ Microbiol 67: 2723-2733.
66. Šimek K, Weinabeur M, Horňák K, Jezbera J, Nedoma J, Dolan JR (2007) Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community. Environ Microbiol 9: 789-800.
67. Sime-Ngando T, Pradeep Ram AS (2005) Grazers effects on prokaryotes and viruses in a freshwater microcosm experiment. Aquat Microb Ecol 41: 115-124.
68. Snyder AR, Williams HN, Baer ML, Walker KE, Stine OC (2002) 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int J Syst Evol Microbiol 52: 2089-2094.
69. Solé RV, Bascompte J (2006) Self-organization in complex ecosystems. Princeton University Press, Princeton.
70. Steward GF, Smith DC, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Mar Ecol Prog Ser 131: 287-300.
71. Strom SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 351-386.
72. Suttle CA (2007) Marine viruses-major players in global ecosystem. Nat Rev Microbiol 5: 801-812.
73. Suttle CA, Cheng F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58: 3721-3729.
74. Tanaka T, Rassoulzadegan F (2002) Full-depth profile (0-2000 m) of bacteria, heterotrophic nanoflagellates and ciliates in the NW Mediterranean Sea: vertical portioning of microbial trophic structures. Deep Sea Res II 49: 2093-2107.
75. Thingstad TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320-1328.
76. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13: 19-27.
77. Utsumi S, Ando Y, Miki T (2010) Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Popul Ecol. doi: 10. 1007/s10144-010-0237-2.
78. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181.
79. Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64: 431-438.
80. Weinbauer MG, Christaki U, Nedoma J, Šimek K (2003) Comparing the effects of resource enrichment and grazing on viral production in a meso-eutrophic reservoir. Aquat Microb Ecol 31: 137-144.
81. Weinbauer MG, Horňák JK, Nedoma J, Dolan JR, Šimek K (2007) Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environ Microbiol 9: 777-788.
82. Williamson SJ, Houchin LA, McDaniel L, Paul JH (2002) Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68: 4307-4314.
83. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69-114.
84. Yair S, Yaacov D, Susan K, Jurkevitch E (2003) Small eats big: ecology and diversity of Bdellovibrio and like organisms, and their dynamics in predator-prey interactions. Agronomie 23: 433-440.
85. Zhang R, Weinbauer M, Qian OY (2007) Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters. Environ Microbiol 9: 3008-3018.