A microbial perspective on biological invasions in aquatic ecosystems

Hydrobiologia

Volumn 746, Issue 1, 2015, Pages 13-22

  Amalfitano, Stefano ^a   Coci, Manuela ^b,c   Corno, Gianluca ^c   Luna, Gian Marco ^d  

^a WATER RESEARCH INSTITUTE   (Italy)

^b Microb co   (Italy)

^c Microbial Ecology Group   (Italy)

^d CNR   (Italy)

Author keywords

Bacteria; Invasibility; Invasiveness; Microbial community; Pathogens

Indexed keywords

EID: 84939896707     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-014-2002-6     Document Type: Article

References (97)

1. Amend, A. S., T. A. Oliver, L. A. Amaral-Zettler, A. Boetius, J. A. Fuhrman, M. C. Horner-Devine, S. M. Huse, D. B. M. Welch, A. C. Martiny, A. Ramette, L. Zinger, M. L. Sogin & J. B. H. Martiny, 2013. Macroecological patterns of marine bacteria on a global scale. Journal of Biogeography 40: 800–811.
2. Barberan, A., E. O. Casamayor & N. Fierer, 2014. The microbial contribution to macroecology. Frontiers in Microbiology 5: e203.
3. Becks, L., F. M. Hilker, H. Malchow, K. Jurgens & H. Arndt, 2005. Experimental demonstration of chaos in a microbial food web. Nature 435: 1226–1229.
4. Blokesch, M. & G. K. Schoolnik, 2007. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLOS Pathogens 3: 733–742.
5. Blom, J. F. & J. Pernthaler, 2010. Antibiotic effects of three strains of chrysophytes (Ochromonas, Poterioochromonas) on freshwater bacterial isolates. FEMS Microbiology Ecology 71: 281–290.
6. Bohannan, B. J. M. & R. E. Lenski, 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3: 362–377.
7. Bollens, S. M., J. R. Cordell, S. Avent & R. Hooff, 2002. Zooplankton invasions: a brief review, plus two case studies from the northeast Pacific Ocean. Hydrobiologia 480: 87–110.
8. Callieri, C., G. Corno & R. Bertoni, 2006. Bacterial grazing by mixotrophic flagellates and Daphnia longispina: a comparison in a fishless alpine lake. Aquatic Microbial Ecology 42: 127–137.
9. Capdevila-Arguelles, L. & B. Zilletti, 2010. A perspective on climate change and invasive alien species. Council of Europe Nature and Environment Series 156: 365–417.
10. Chakraborty, A. & B. L. Li, 2010. The role of fluctuating resource supply in a habitat maintained by the competition-colonization trade-off. In Li, B. L. (ed.) Ecological Complexity and Sustainability. Annals of the New York Academy of Sciences 1195: 27–39.
11. Chave, J., H. C. Muller-Landau & S. A. Levin, 2002. Comparing classical community models: theoretical consequences for patterns of diversity. American Naturalist 159: 1–23.
12. Colautti, R. I., I. A. Grigorovich & H. J. MacIsaac, 2006. Propagule pressure: a null model for biological invasions. Biological Invasions 8: 1023–1037.
13. Corno, G., 2006. Effects of nutrient availability and Ochromonas sp predation on size and composition of a simplified aquatic bacterial community. FEMS Microbiology Ecology 58: 354–363.
14. Corno, G. & K. Juergens, 2008. Structural and functional patterns of bacterial communities in response to protist predation along an experimental productivity gradient. Environmental Microbiology 10: 2857–2871.
15. Corno, G., E. Caravati, C. Callieri & R. Bertoni, 2008. Effects of predation pressure on bacterial abundance, diversity, and size-structure distribution in an oligotrophic system. Journal of Limnology 67: 107–119.
16. Corno, G., J. Villiger & J. Pernthaler, 2013. Coaggregation in a microbial predator-prey system affects competition and trophic transfer efficiency. Ecology 94: 870–881.
17. Croswell, A., E. Amir, P. Teggatz, M. Barman & N. H. Salzman, 2009. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric salmonella infection. Infection and Immunity 77: 2741–2753.
18. Davis, M. A. & M. Pelsor, 2001. Experimental support for a resource-based mechanistic model of invasibility. Ecology Letters 4: 421–428.
19. Davis, M. A., J. P. Grime & K. Thompson, 2000. Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88: 528–534.
20. Diehl, S. & M. Feissel, 2001. Intraguild prey suffer from enrichment of their resources: a microcosm experiment with ciliates. Ecology 82: 2977–2983.
21. Drake, L. A., M. A. Doblin & F. C. Dobbs, 2007. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Marine Pollution Bulletin 55: 333–341.
22. Dukes, J. S., 2001. Biodiversity and invasibility in grassland microcosms. Oecologia 126: 563–568.
23. Eisenhauer, N., A. Milcu, A. C. W. Sabais & S. Scheu, 2008. Animal ecosystem engineers modulate the diversity-invasibility relationship. PLOS One 3: e3489.
24. Eisenhauer, N., S. Scheu & A. Jousset, 2012. Bacterial diversity stabilizes community productivity. PLOS One 7: e34517.
25. Eisenhauer, N., W. Schulz, S. Scheu & A. Jousset, 2013. Niche dimensionality links biodiversity and invasibility of microbial communities. Functional Ecology 27: 282–288.
26. Fargione, J. E. & D. Tilman, 2005. Diversity decreases invasion via both sampling and complementarity effects. Ecology Letters 8: 604–611.
27. Fazi, S., S. Amalfitano, C. Piccini, A. Zoppini, A. Puddu & J. Pernthaler, 2008. Colonization of overlaying water by bacteria from dry river sediments. Environmental Microbiology 10: 2760–2772.
28. Fischbach, M. A. & C. T. Walsh, 2009. Antibiotics for emerging pathogens. Science 325: 1089–1093.
29. Fridley, J. D., J. J. Stachowicz, S. Naeem, D. F. Sax, E. W. Seabloom, M. D. Smith, T. J. Stohlgren, D. Tilman & B. Von Holle, 2007. The invasion paradox: reconciling pattern and process in species invasions. Ecology 88: 3–17.
30. Friman, V. P., A. Jousset & A. Buckling, 2014. Rapid prey evolution can alter the structure of predator-prey communities. Journal of Evolutionary Biology 27: 374–380.
31. Gatto, M., L. Mari, E. Bertuzzo, R. Casagrandi, L. Righetto, I. Rodriguez-Iturbe & A. Rinaldo, 2013. Spatially explicit conditions for waterborne pathogen invasion. American Naturalist 182: 328–346.
32. Gherardi, F., 2006. Crayfish invading Europe: the case study of Procambarus clarkii. Marine and Freshwater Behaviour and Physiology 39: 175–191.
33. Gibbons, S. M., J. G. Caporaso, M. Pirrung, D. Field, R. Knight & J. A. Gilbert, 2013. Evidence for a persistent microbial seed bank throughout the global ocean. Proceedings of the National Academy of Sciences of the United States of America 110: 4651–4655.
34. Gilbert, J. A., D. Field, P. Swift, S. Thomas, D. Cummings, B. Temperton, K. Weynberg, S. Huse, M. Hughes, I. Joint, P. J. Somerfield & M. Muehling, 2010. The taxonomic and functional diversity of microbes at a temperate coastal site: a “multi-omic” study of seasonal and diel temporal variation. PLOS One 5: e15545.
35. Hanson, C. A., J. A. Fuhrman, M. C. Horner-Devine & J. B. H. Martiny, 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nature Reviews Microbiology 10: 497–506.
36. Hodgson, D. J., P. B. Rainey & A. Buckling, 2002. Mechanisms linking diversity, productivity and invasibility in experimental bacterial communities. Proceedings of the Royal Society B 269: 2277–2283.
37. Hooper, D. U., F. S. Chapin, J. J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J. H. Lawton, D. M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setala, A. J. Symstad, J. Vandermeer & D. A. Wardle, 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.
38. Hooper, D. U., E. C. Adair, B. J. Cardinale, J. E. K. Byrnes, B. A. Hungate, K. L. Matulich, A. Gonzalez, J. E. Duffy, L. Gamfeldt & M. I. O’Connor, 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486: 105–129.
39. Hornak, K. & G. Corno, 2012. Every coin has a back side: invasion by Limnohabitans planktonicus promotes the maintenance of species diversity in bacterial communities. PLOS One 7: e51576.
40. Hulme, P. E., W. Nentwig, P. Pysek & M. Vila, 2010. DAISIE: Delivering Alien Invasive Species Inventories for Europe. Atlas of Biodiversity Risk: 134–135.
41. Huston, M. A., 1997. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110: 449–460.
42. Jessup, C. M., S. E. Forde & B. J. M. Bohannan, 2005. Microbial experimental systems in ecology. Advances in Ecological Research 37: 273–307.
43. Jiang, L. & P. J. Morin, 2004. Productivity gradients cause positive diversity–invasibility relationships in microbial communities. Ecology Letters 7: 1047–1057.
44. Jousset, A., N. Eisenhauer, E. Materne & S. Scheu, 2013. Evolutionary history predicts the stability of cooperation in microbial communities. Nature Communications 4: e3573.
45. Jousset, A., B. Schmid, S. Scheu & N. Eisenhauer, 2011a. Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecology Letters 14: 537–545.
46. Jousset, A., W. Schulz, S. Scheu & N. Eisenhauer, 2011b. Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME Journal 5: 1108–1114.
47. Keane, R. M. & M. J. Crawley, 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17: 164–170.
48. Kuemmerer, K., 2009. Antibiotics in the aquatic environment – a review – part I. Chemosphere 75: 417–434.
49. Ladau, J., T. J. Sharpton, M. M. Finucane, G. Jospin, S. W. Kembel, J. O’Dwyer, A. F. Koeppel, J. L. Green & K. S. Pollard, 2013. Global marine bacterial diversity peaks at high latitudes in winter. ISME Journal 7: 1669–1677.
50. Langenheder, S., M. T. Bulling, M. Solan & J. I. Prosser, 2010. Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLOS One 5: e10834.
51. Lawrence, J. E., 2008. Furtive foes: algal viruses as potential invaders. Ices Journal of Marine Science 65: 716–722.
52. Lennon, J. T. & S. E. Jones, 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Reviews Microbiology 9: 119–130.
53. Levine, J. M., 2000. Species diversity and biological invasions: relating local process to community pattern. Science 288: 852–854.
54. Li, W. & M. H. H. Stevens, 2012. Fluctuating resource availability increases invasibility in microbial microcosms. Oikos 121: 435–441.
55. Lindstrom, E. S. & O. Ostman, 2011. The importance of dispersal for bacterial community composition and functioning. PLOS One 6: e25883.
56. Litchman, E., 2010. Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecology Letters 13: 1560–1572.
57. Lodge, D. M., 1993. Biological invasions – lessons for ecology. Trends in Ecology & Evolution 8: 133–137.
58. Logares, R., E. S. Lindstrom, S. Langenheder, J. B. Logue, H. Paterson, J. Laybourn-Parry, K. Rengefors, L. Tranvik & S. Bertilsson, 2013. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME Journal 7: 937–948.
59. Loreau, M. & N. Mouquet, 1999. Immigration and the maintenance of local species diversity. American Naturalist 154: 427–440.
60. Luna, G. M., C. Vignaroli, C. Rinaldi, A. Pusceddu, L. Nicoletti, M. Gabellini, R. Danovaro & F. Biavasco, 2010. Extraintestinal Escherichia coli carrying virulence genes in coastal marine sediments. Applied and Environmental Microbiology 76: 5659–5668.
61. McGeoch, M. A., D. Spear, E. J. Kleynhans & E. Marais, 2012. Uncertainty in invasive alien species listing. Ecological Applications 22: 959–971.
62. Meinesz, A., J. Devaugelas, B. Hesse & X. Mari, 1993. Spread of the introduced tropical green-alga Caulerpa taxifolia in northern mediterranean waters. Journal of Applied Phycology 5: 141–147.
63. Molnar, J. L., R. L. Gamboa, C. Revenga & M. D. Spalding, 2008. Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment 6: 485–492.
64. Morin, P., 1999. Productivity, intraguild predation, and population dynamics in experimental food webs. Ecology 80: 752–760.
65. Naeem, S., 2008. Advancing realism in biodiversity research. Trends in Ecology & Evolution 23: 414–416.
66. Nogales, B., M. P. Lanfranconi, J. M. Pina-Villalonga & R. Bosch, 2011. Anthropogenic perturbations in marine microbial communities. FEMS Microbiology Reviews 35: 275–298.
67. Pedros-Alio, C., 2006. Marine microbial diversity: can it be determined? Trends in Microbiology 14: 257–263.
68. Pedros-Alio, C., 2012. The rare bacterial biosphere. Annual Review of Marine Science 4: 449–466.
69. Pernthaler, J., 2005. Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3: 537–546.
70. Perrings, C., K. Dehnen-Schmutz, J. Touza & M. Williamson, 2005. How to manage biological invasions under globalization. Trends in Ecology & Evolution 20: 212–215.
71. Peter, H., S. Beier, S. Bertilsson, E. S. Lindstrom, S. Langenheder & L. J. Tranvik, 2011. Function-specific response to depletion of microbial diversity. ISME Journal 5: 351–361.
72. Pimentel, D., L. Lach, R. Zuniga & D. Morrison, 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50: 53–65.
73. Price, J. E. & P. J. Morin, 2004. Colonization history determines alternate community states in a food web of intraguild predators. Ecology 85: 1017–1028.
74. Proia, L., G. Lupini, V. Osorio, S. Perez, D. Barcelo, T. Schwartz, S. Amalfitano, S. Fazi, A. M. Romani & S. Sabater, 2013. Response of biofilm bacterial communities to antibiotic pollutants in a Mediterranean river. Chemosphere 92: 1126–1135.
75. Randolph, S. E. & D. J. Rogers, 2010. The arrival, establishment and spread of exotic diseases: patterns and predictions. Nature Reviews Microbiology 8: 361–371.
76. Ricciardi, A., M. F. Hoopes, M. P. Marchetti & J. L. Lockwood, 2013. Progress toward understanding the ecological impacts of nonnative species. Ecological Monographs 83: 263–282.
77. Rosindell, J., S. P. Hubbell & R. S. Etienne, 2011. The unified neutral theory of biodiversity and biogeography at age ten. Trends in Ecology & Evolution 26: 340–348.
78. Severin, I., O. Ostman & E. S. Lindstrom, 2013. Variable effects of dispersal on productivity of bacterial communities due to changes in functional trait composition. PLOS One 8: e80825.
79. Simberloff, D., L. Souza, M. A. Nunez, M. N. Barrios-Garcia & W. Bunn, 2012. The natives are restless, but not often and mostly when disturbed. Ecology 93: 598–607.
80. Shade, A., H. Peter, S. D. Allison, D. L. Baho, M. Berga, H. Burgmann, D. H. Huber, S. Langenheder, J. T. Lennon, J. B. H. Martiny, K. L. Matulich, T. M. Schmidt & J. Handelsman, 2012. Fundamentals of microbial community resistance and resilience. Frontiers in Microbiology 3: e417.
81. Stoll, C., J. P. S. Sidhu, A. Tiehm & S. Toze, 2012. Prevalence of clinically relevant antibiotic resistance genes in surface water samples collected from Germany and Australia. Environmental Science & Technology 46: 9716–9726.
82. Taylor, B. W. & M. L. Bothwell, 2014. The origin of invasive microorganisms matters for science, policy, and management: the case of Didymosphenia geminata. Bioscience 64: 531–538.
83. Thingstad, T. F., 2000. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnology and Oceanography 45: 1320–1328.
84. Tilman, D., 1999. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80: 1455–1474.
85. Torsvik, V., L. Ovreas & T. F. Thingstad, 2002. Prokaryotic diversity – magnitude, dynamics, and controlling factors. Science 296: 1064–1066.
86. van der Putten, W. H., J. N. Klironomos & D. A. Wardle, 2007. Microbial ecology of biological invasions. ISME Journal 1: 28–37.
87. van Elsas, J. D., M. Chiurazzi, C. A. Mallon, D. Elhottova, V. Kristufek & J. F. Salles, 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences of the United States of America 109: 1159–1164.
88. Vezzulli, L., I. Brettar, E. Pezzati, P. C. Reid, R. R. Colwell, M. G. Hoefle & C. Pruzzo, 2012. Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME Journal 6: 21–30.
89. Vezzulli, L., R. R. Colwell & C. Pruzzo, 2013. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microbial Ecology 65: 817–825.
90. Vitousek, P. M., C. M. Dantonio, L. L. Loope & R. Westbrooks, 1996. Biological invasions as global environmental change. American Scientist 84: 468–478.
91. Walther, B. A. & P. W. Ewald, 2004. Pathogen survival in the external environment and the evolution of virulence. Biological Reviews 79: 849–869.
92. Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J. M. Fromentin, O. Hoegh-Guldberg & F. Bairlein, 2002. Ecological responses to recent climate change. Nature 416: 389–395.
93. Winter, C., T. Bouvier, M. G. Weinbauer & T. F. Thingstad, 2010. Trade-offs between competition and defense specialists among unicellular planktonic organisms: the “Killing the Winner” hypothesis revisited. Microbiology and Molecular Biology Reviews 74: 42–57.
94. Xu, J. P., 2006. Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Molecular Ecology 15: 1713–1731.
95. Yang, L. H., J. L. Bastow, K. O. Spence & A. N. Wright, 2008. What can we learn from resource pulses? Ecology 89: 621–634.
96. Zinger, L., A. Gobet & T. Pommier, 2012. Two decades of describing the unseen majority of aquatic microbial diversity. Molecular Ecology 21: 1878–1896.
97. Zoppini, A., N. Ademollo, S. Amalfitano, P. Casella, L. Patrolecco & S. Polesello, 2014. Organic priority substances and microbial processes in river sediments subject to contrasting hydrological conditions. Science of the total environment 484: 74–83.