Microbial invasions in terrestrial ecosystems


Human travel and global trade have tremendously increased the spread of invasive microorganisms in new regions. Experimental and observational studies in terrestrial ecosystems are beginning to shed light on processes of microbial invasions, their ecological impacts and implications for ecosystem functioning. We provide examples of terrestrial invasive microorganisms, including bacteria, fungi, oomycetes and other protists, and viruses, and discuss the impacts of pathogenic and non-pathogenic invasive microorganisms at levels ranging from host species to ecosystems. This Review highlights that despite the recent progress in microbial invasion research, we are only beginning to understand how alien microorganisms interact with native microorganisms, and the implications of those interactions. Finally, we propose three research themes — microbial interactions, impacts and climate change — to make microbial invasion research a truly integrative discipline.

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Fig. 1: Examples of invasive microorganisms that cause tree diseases.
Fig. 2: The microbial invasion process and potential impacts.
Fig. 3: Pathways of spillover of alien pathogenic microorganisms.


  1. 1.

    Chapman, D., Purse, B. V., Roy, H. E. & Bullock, J. M. Global trade networks determine the distribution of invasive non-native species. Glob. Ecol. Biogeogr. 26, 907–917 (2017).

  2. 2.

    Sikes, B. A. et al. Import volumes and biosecurity interventions shape the arrival rate of fungal pathogens. PLOS Biol. 16, e2006025 (2018).

  3. 3.

    Weiss, H. et al. The airplane cabin microbiome. Microb. Ecol. 77, 87–95 (2018).

  4. 4.

    Santini, A., Liebhold, A., Migliorini, D. & Woodward, S. Tracing the role of human civilization in the globalization of plant pathogens. ISME J. 12, 647–652 (2018).

  5. 5.

    Bebber, D. P., Ramotowski, M. A. T. & Gurr, S. J. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3, 985–988 (2013).

  6. 6.

    Hulme, P. E. Climate change and biological invasions: evidence, expectations, and response options. Biol. Rev. 92, 1297–1313 (2017).

  7. 7.

    Ricciardi, A. et al. Invasion science: a horizon scan of emerging challenges and opportunities. Trends Ecol. Evol. 32, 464–474 (2017).

  8. 8.

    Gladieux, P. et al. The population biology of fungal invasions. Mol. Ecol. 24, 1969–1986 (2015).

  9. 9.

    Desprez-Loustau, M. L. et al. The fungal dimension of biological invasions. Trends Ecol. Evol. 22, 472–480 (2007). This review is one of the first to highlight the potential invasion mechanisms and impacts of both pathogenic and non-pathogenic fungi.

  10. 10.

    Judelson, H. S. & Blanco, F. A. The spores of Phytophthora: weapons of the plant destroyer. Nat. Rev. Microbiol. 3, 47–58 (2005). This Review provides an overview of several pathogenesis strategies of Phytophthora.

  11. 11.

    Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463 (2019).

  12. 12.

    Richardson, D. M. et al. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6, 93–107 (2000).

  13. 13.

    Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).

  14. 14.

    Essl, F. et al. Which taxa are alien? Criteria, applications, and uncertainties. Bioscience 68, 496–509 (2018).

  15. 15.

    Convention on Biological Diversity. COP 5 decision V/8: alien species that threaten ecosystems, habitats or species. CBD https://www.cbd.int/decision/cop/default.shtml?id=7150 (2000).

  16. 16.

    Zenni, R. D. & Nuñez, M. A. The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122, 801–815 (2013).

  17. 17.

    Daszak, P., Cunningham, A. & Hyatt, A. Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449 (2000).

  18. 18.

    Kolar, C. S. & Lodge, D. M. Progress in invasion biology. Trends Ecol. Evol. 16, 199–204 (2001).

  19. 19.

    van Kleunen, M., Bossdorf, O. & Dawson, W. The ecology and evolution of alien plants. Annu. Rev. Ecol. Evol. Syst. 49, 25–47 (2018).

  20. 20.

    Jeschke, J. et al. Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14, 1–20 (2012).

  21. 21.

    Turbelin, A. J., Malamud, B. D. & Francis, R. A. Mapping the global state of invasive alien species: patterns of invasion and policy responses. Glob. Ecol. Biogeogr. 26, 78–92 (2017).

  22. 22.

    Dickie, I., Bolstridge, N., Cooper, J. & Peltzer, D. Co-invasion by Pinus and its mycorrhizal fungi. New Phytol. 187, 475–484 (2010). This study shows co-invasion of Pinus trees and their associated mycorrhizal fungi in New Zealand.

  23. 23.

    Mallon, C., Van Elsas, J. & Salles, J. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol. 23, 719–729 (2015).

  24. 24.

    Van der Putten, W. H., Klironomos, J. N. & Wardle, D. A. Microbial ecology of biological invasions. ISME J. 1, 28–37 (2007).

  25. 25.

    Dickie, I. A. et al. The emerging science of linked plant–fungal invasions. New Phytol. 215, 1314–1332 (2017).

  26. 26.

    Vellinga, E., Wolfe, B. & Pringle, A. Global patterns of ectomycorrhizal introductions. New Phytol. 181, 960–973 (2009). This global analysis provides a list of ectomycorrhizal introductions.

  27. 27.

    Lymbery, A. J., Morine, M., Kanani, H. G., Beatty, S. J. & Morgan, D. L. Co-invaders: the effects of alien parasites on native hosts. Int. J. Parasitol. Parasites Wildl. 3, 171–177 (2014).

  28. 28.

    Correia, M., Heleno, R., da Silva, L. P., Costa, J. M. & Rodríguez-Echeverría, S. First evidence for the joint dispersal of mycorrhizal fungi and plant diaspores by birds. New Phytol. 222, 1054–1060 (2019).

  29. 29.

    Nuñez, M. A. et al. Exotic mammals disperse exotic fungi that promote invasion by exotic trees. PLOS ONE 8, e66832 (2013).

  30. 30.

    Mitchell, C. & Torchin, M. Parasites, pathogens, and invasions by plants and animals. Front. Ecol. Environ. 2, 183–190 (2004).

  31. 31.

    Amsellem, L. et al. Importance of microorganisms to macroorganisms invasions. Adv. Ecol. Res. 57, 99–146 (2017).

  32. 32.

    Banks, N. C., Paini, D. R., Bayliss, K. L. & Hodda, M. The role of global trade and transport network topology in the human-mediated dispersal of alien species. Ecol. Lett. 18, 188–199 (2015).

  33. 33.

    Dutech, C. et al. The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol. Ecol. 21, 3931–3946 (2012). This study reveals that C. parasitica became invasive in North America and western Europe owing to multiple introduction events.

  34. 34.

    Rigling, D. & Prospero, S. Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol. Plant Pathol. 19, 7–20 (2018).

  35. 35.

    Young, H. S., Parker, I. M., Gilbert, G. S., Sofia Guerra, A. & Nunn, C. L. Introduced species, disease ecology, and biodiversity–disease relationships. Trends Ecol. Evol. 32, 41–54 (2017).

  36. 36.

    Parker, I. & Gilbert, G. The evolutionary ecology of novel plant-pathogen interactions. Annu. Rev. Ecol. Evol. Syst. 35, 675–700 (2004).

  37. 37.

    Anderson, R. & May, R. The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos. Trans. R. Soc. Lond. B 314, 533–570 (1986).

  38. 38.

    Melotto, M., Underwood, W., Koczan, J., Nomura, K. & He, S. Y. Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969–980 (2006).

  39. 39.

    Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).

  40. 40.

    Tyler, B. M. et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313, 1261–1266 (2006).

  41. 41.

    Grunwald, N., Goss, E. & Press, C. Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Mol. Plant Pathol. 9, 729–740 (2008).

  42. 42.

    Elton, C. The Ecology of Invasions by Animals and Plants (Methuen, 1958).

  43. 43.

    Levine, J. Species diversity and biological invasions: relating local process to community pattern. Science 288, 852–854 (2000).

  44. 44.

    van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl Acad. Sci. USA 109, 1159–1164 (2012).

  45. 45.

    Eisenhauer, N., Schulz, W., Scheu, S. & Jousset, A. Niche dimensionality links biodiversity and invasibility of microbial communities. Funct. Ecol. 27, 282–288 (2013).

  46. 46.

    Lockwood, J. L., Cassey, P. & Blackburn, T. The role of propagule pressure in explaining species invasions. Trends Ecol. Evol. 20, 223–228 (2005).

  47. 47.

    Acosta, F., Zamor, R. M., Najar, F. Z., Roe, B. A. & Hambright, K. D. Dynamics of an experimental microbial invasion. Proc. Natl Acad. Sci. USA 112, 11594–11599 (2015).

  48. 48.

    Haas, S. E., Hooten, M. B., Rizzo, D. M. & Meentemeyer, R. K. Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol. Lett. 14, 1108–1116 (2011). This study confirmed diversity–invasibility relationships for a plant pathogen from a field study.

  49. 49.

    Vilà, M. et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011).

  50. 50.

    Cameron, E. K., Vilà, M. & Cabeza, M. Global meta-analysis of the impacts of terrestrial invertebrate invaders on species, communities and ecosystems. Glob. Ecol. Biogeogr. 25, 596–606 (2016).

  51. 51.

    Litchman, E. Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol. Lett. 13, 1560–1572 (2010).

  52. 52.

    Brader, G. et al. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu. Rev. Phytopathol. 55, 61–83 (2017).

  53. 53.

    Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

  54. 54.

    Jung, T., Colquhoun, I. J. & Hardy, G. E. S. J. New insights into the survival strategy of the invasive soilborne pathogen Phytophthora cinnamomi in different natural ecosystems in Western Australia. For. Pathol. 43, 266–288 (2013).

  55. 55.

    Hee, W. Y., Torreña, P. S., Blackman, L. M. & Hardham, A. R. in Phytophthora: A Global Perspective Vol. 2 (ed. Lamour, K.) 124 (CABI, 2013).

  56. 56.

    Day, N. J., Dunfield, K. E. & Antunes, P. M. Fungi from a non-native invasive plant increase its growth but have different growth effects on native plants. Biol. Invasions 18, 231–243 (2016).

  57. 57.

    Simberloff, D. & Von Holle, B. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions 1, 21–32 (1999).

  58. 58.

    Reisen, W. K. Landscape epidemiology of vector-borne diseases. Annu. Rev. Entomol. 55, 461–483 (2010).

  59. 59.

    Taerum, S. J. et al. Putative origins of the fungus Leptographium procerum. Fungal Biol. 121, 82–94 (2017).

  60. 60.

    Lorch, J. M. et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378 (2011).

  61. 61.

    Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl Acad. Sci. USA 109, 6999–7003 (2012).

  62. 62.

    Zukal, J. et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci. Rep. 6, 19829 (2016).

  63. 63.

    Rodríguez-Echeverría, S. Rhizobial hitchhikers from down under: invasional meltdown in a plant-bacteria mutualism? J. Biogeogr. 37, 1611–1622 (2010). This article reveals invasional meltdown in plant–microorganism interactions.

  64. 64.

    Kamutando, C. N. et al. The functional potential of the rhizospheric microbiome of an invasive tree species, Acacia dealbata. Microb. Ecol. 77, 191–200 (2019).

  65. 65.

    Klironomos, J. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292–2301 (2003). This study is one of the first to show differences in plant responses to alien and native arbuscular mycorrhizal fungi.

  66. 66.

    Chalkowski, K., Lepczyk, C. A. & Zohdy, S. Parasite ecology of invasive species: conceptual framework and new hypotheses. Trends Parasitol. 34, 655–663 (2018).

  67. 67.

    Johnson, P. T. J., De Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).

  68. 68.

    Parker, I. M. et al. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520, 542–544 (2015). This study shows how community characteristics can influence disease outcomes.

  69. 69.

    Li, S.-P., Tan, J., Yang, X., Ma, C. & Jiang, L. Niche and fitness differences determine invasion success and impact in laboratory bacterial communities. ISME J. 13, 402–412 (2019).

  70. 70.

    Kinnunen, M., Dechesne, A., Albrechtsen, H.-J. & Smets, B. F. Stochastic processes govern invasion success in microbial communities when the invader is phylogenetically close to resident bacteria. ISME J. 12, 2748–2756 (2018).

  71. 71.

    Van Kleunen, M., Weber, E. & Fischer, M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 13, 235–245 (2010).

  72. 72.

    McCary, M. A., Mores, R., Farfan, M. A. & Wise, D. H. Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: a meta-analysis. Ecol. Lett. 19, 328–335 (2016).

  73. 73.

    Vitousek, P. & Walker, L. Biological invasion by Myrica Faya in Hawaii: plant demography, nitrogen fixation, ecosystem effects. Ecol. Monogr. 59, 247–265 (1989).

  74. 74.

    Spoel, S. H. & Dong, X. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12, 89–100 (2012).

  75. 75.

    Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).

  76. 76.

    Newman, M., Barbási, A.-L. & Watts, D. The Structure and Dynamics of Networks (Princeton Univ. Press, 2011).

  77. 77.

    Delmas, E. et al. Analysing ecological networks of species interactions. Biol. Rev. 94, 16–36 (2019).

  78. 78.

    Ramirez, K. S., Geisen, S., Morriën, E., Snoek, B. L. & van der Putten, W. H. Network analyses can advance above-belowground ecology. Trends Plant Sci. 23, 759–768 (2018).

  79. 79.

    Tylianakis, J. M. & Morris, R. J. Ecological networks across environmental gradients. Annu. Rev. Ecol. Evol. Syst. 48, 25–48 (2017).

  80. 80.

    McGeoch, M. A. et al. Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers. Distrib. 16, 95–108 (2010).

  81. 81.

    Diaz, S. et al. Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES, 2019).

  82. 82.

    Roy, H. E. et al. Alien pathogens on the horizon: opportunities for predicting their threat to wildlife. Conserv. Lett. 10, 476–483 (2017).

  83. 83.

    Rizzo, D. M. & Garbelotto, M. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1, 197–204 (2003).

  84. 84.

    Wingfield, M. J. et al. Novel and co-evolved associations between insects and microorganisms as drivers of forest pestilence. Biol. Invasions 18, 1045–1056 (2016).

  85. 85.

    Dunn, A. M. & Hatcher, M. J. Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol. 31, 189–199 (2015).

  86. 86.

    Tedersoo, L., Tooming-Klunderud, A. & Anslan, S. Methods PacBio metabarcoding of fungi and other eukaryotes: errors, biases and perspectives. New Phytol. 217, 1370–1385 (2017).

  87. 87.

    Koskella, B., Hall, L. J. & Metcalf, C. J. E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat. Ecol. Evol. 1, 1606–1615 (2017).

  88. 88.

    Hanlon, S. J. O. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 627, 621–627 (2018). This study uses whole-genome sequencing of chytrid fungi to estimate spatiotemporal origins.

  89. 89.

    Jeschke, J. M. General hypotheses in invasion ecology. Divers. Distrib. 20, 1229–1234 (2014).

  90. 90.

    Milgroom, M. Population Biology of Plant Pathogens: Genetics, Ecology and Evolution (The American Phytopathological Society, 2015).

  91. 91.

    Gilligan, C. A. & van den Bosch, F. Epidemiological models for invasion and persistence of pathogens. Annu. Rev. Phytopathol. 46, 385–418 (2008).

  92. 92.

    Madigan, M., Bender, K., Buckley, D., Sattley, W. & Stahl, D. Brock Biology of Microorganisms 15th edn (Pearson Education Limited, 2019).

  93. 93.

    Ribet, D. & Cossart, P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 17, 173–183 (2015).

  94. 94.

    Mazza, G., Tricarico, E., Genovesi, P. & Gherardi, F. Biological invaders are threats to human health: an overview. Ethol. Ecol. Evol. 26, 112–129 (2014).

  95. 95.

    Hulme, P. Invasive species challenge the global response to emerging diseases. Trends Parasitol. 30, 267–270 (2014).

  96. 96.

    Paupy, C., Delatte, H., Bagny, L., Corbel, V. & Fontenille, D. Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes Infect. 11, 1177–1185 (2009).

  97. 97.

    Anda, P. et al. Waterborne outbreak of tularemia associated with crayfish fishing. Emerg. Infect. Dis. 7, 575–582 (2001).

  98. 98.

    Mazza, G. & Tricarcio, E. (eds) Invasive Species and Human Health (CABI, 2018).

  99. 99.

    Amalfitano, S., Coci, M., Corno, G. & Luna, G. M. A microbial perspective on biological invasions in aquatic ecosystems. Hydrobiologia 746, 13–22 (2014).

  100. 100.

    Harvell, C. et al. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162 (2002).

  101. 101.

    Verant, M. L., Boyles, J. G., Waldrep, W., Wibbelt, G. & Blehert, D. S. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat White-nose syndrome. PLOS ONE 7, e46280 (2012).

  102. 102.

    O’connor, M. I. & Bernhardt, J. R. The metabolic theory of ecology and the cost of parasitism. PLOS Biol. 16, e2005628 (2018).

  103. 103.

    Cohen, J. M. et al. The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecol. Lett. 20, 184–193 (2017).

  104. 104.

    Clare, F. C. et al. Climate forcing of an emerging pathogenic fungus across a montane multi-host community. Philos. Trans. R. Soc. B 371, 20150454 (2016).

  105. 105.

    Mckinney, L., Thomsen, I., Kjær, E., Bengtsson, S. & Nielsen, L. Rapid invasion by an aggressive pathogenic fungus (Hymenoscyphus pseudoalbidus) replaces a native decomposer (Hymenoscyphus albidus): a case of local cryptic extinction? Fungal Ecol. 5, 663–669 (2012).

  106. 106.

    Kozanitas, M., Osmundson, T. W., Linzer, R. & Garbelotto, M. Interspecific interactions between the sudden oak death pathogen Phytophthora ramorum and two sympatric Phytophthora species in varying ecological conditions. Fungal Ecol. 28, 86–96 (2017).

  107. 107.

    Rizzo, D. M., Garbelotto, M. & Hansen, E. M. Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu. Rev. Phytopathol. 43, 309–335 (2005).

  108. 108.

    Grünwald, N. J., Garbelotto, M., Goss, E. M., Heungens, K. & Prospero, S. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol. 20, 131–138 (2012).

  109. 109.

    Hardham, A. & Blackman, L. Phytophthora cinnamomi. Mol. Plant Pathol. 19, 260–285 (2018).

  110. 110.

    Robin, C. et al. Root and aerial infections of Chamaecyparis lawsoniana by Phytophthora lateralis: a new threat for European countries. For. Pathol. 41, 417–424 (2011).

  111. 111.

    Thoirain, B., Husson, C. & Marçais, B. Risk factors for the Phytophthora -induced decline of alder in northeastern France. Phytopathology 97, 99–105 (2007).

  112. 112.

    Zambino, P. J. Biology and pathology of Ribes and their implications for management of white pine blister rust. For. Pathol. 40, 264–291 (2010).

  113. 113.

    Geils, B. & Vogler, D. A. in The Future of High-Elevation, Five-Needle White Pines in Western North America: Proceedings of the High Five Symposium (eds Keane, R., Tomback, D., Murray, M. & Smith, C.) 210–217 (U.S. Department of Agriculture Forest Service, 2011).

  114. 114.

    Kowalski, T. & Holdenrieder, O. Pathogenicity of Chalara fraxinea. For. Pathol. 39, 1–7 (2009).

  115. 115.

    Cleary, M. et al. Friend or foe? Biological and ecological traits of the European ash dieback pathogen Hymenoscyphus fraxineus in its native environment. Sci. Rep. 6, 21895 (2016).

  116. 116.

    Anagnostakis, S. L. Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79, 23–37 (1987).

  117. 117.

    Broders, K., Boraks, A., Barbison, L., Brown, J. & Boland, G. J. Recent insights into the pandemic disease butternut canker caused by the invasive pathogen Ophiognomonia clavigignenti-juglandacearum. For. Pathol. 45, 1–8 (2015).

  118. 118.

    Carnegie, A. J. et al. Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia. Biol. Invasions 18, 127–144 (2016).

  119. 119.

    Carr, D. E. & Banas, L. E. Dogwood anthracnose (Discula destructiva): effects of and consequences for host (Cornus florida) demography. Am. Midl. Nat. 143, 169–177 (2000).

  120. 120.

    Ploetz, R. C. et al. Responses of avocado to laurel wilt, caused by Raffaelea lauricola. Plant Pathol. 61, 801–808 (2012).

  121. 121.

    Juzwik, J., Harrington, T. C., MacDonald, W. L. & Appel, D. N. The origin of Ceratocystis fagacearum, the oak wilt fungus. Annu. Rev. Phytopathol. 46, 13–26 (2008).

  122. 122.

    Wingfield, M. J. et al. Pitch canker caused by Fusarium circinatum – a growing threat to pine plantations and forests worldwide. Australas. Plant Pathol. 37, 319–334 (2008).

  123. 123.

    Garbelotto, M. & Gonthier, P. Biology, epidemiology, and control of Heterobasidion Species worldwide. Annu. Rev. Phytopathol. 51, 39–59 (2013).

  124. 124.

    Brasier, C. in Genetics of Plant Pathogenic Fungi 1st edn Vol. 6 (ed. Sidhu, G. S.) 207–223 (Academic Press, 1988).

  125. 125.

    Comeau, A. M. et al. Functional annotation of the ophiostoma novo-ulmi genome: insights into the phytopathogenicity of the fungal agent of Dutch elm disease. Genome Biol. Evol. 7, 410–430 (2015).

  126. 126.

    Baker, C. J., Harrington, T. C., Krauss, U. & Alfenas, A. C. Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata. Phytopathology 93, 1274–1284 (2003).

  127. 127.

    Muir, J. A. & Cobb, F. W. Infection of radiata and bishop pine by Mycosphaerella pini in California. Can. J. For. Res. 35, 2529–2538 (2005).

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The authors thank K. Steinauer (Netherlands Institute of Ecology) for her suggestions on the manuscript. M.P.T. acknowledges funding from the German Research Foundation (TH 2307/1-1). W.H.v.d.P. acknowledges support from ERC Advanced Grants (ERC-ADV 323020, SPECIALS). S.G. acknowledges funding from the Netherlands Organization for Scientific Research (016.Veni.181.078). This is publication 6755 of the Netherlands Institute of Ecology.

Author information

M.P.T. and S.G. conceived the initial idea and carried out the systematic literature search. All co-authors provided insights to develop the manuscript. M.P.T. wrote the manuscript with inputs from all co-authors.

Correspondence to Madhav P. Thakur.

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The authors declare no competing interests.

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Supplementary information



The second stage in the invasion process, when the alien species arrives in the new environment (including being kept in captivity or cultivation).


The fourth stage after the establishment, in which the alien species disperses to new locations and faces sequential establishment events.


The first stage in the invasion process, when a species is moved outside its known geographic boundary by human agency.


The third stage in the invasion process, when the alien species is able to maintain populations in the new environment over a longer period without direct help of humans.


Simplified ecological units/systems that attempt to mimic some features of ecological systems in laboratory settings.

Spillover effects

The process in which a pathogen of one host infects another host.


The vulnerability of an environment (or a host) to invasion by alien organisms.


The ability of microorganisms to cause disease in a host.

Propagule pressure

The initial size of the introduced population of an alien species in a new environment.

Invasional meltdown

Positive interactions among alien species leading to their invasion success.


Reduction in disease risk due to a greater diversity of hosts.


A measure of biological diversity based on the quantification of how equal the community is in terms of abundance across species.

Adaptive immunity

The acquired ability of an infected host to recognize and destroy the pathogen.

Community modules

Configurations of species interactions within a community, such as predator–prey or host–pathogen pairs.


Collection of units (such as species or taxa) potentially interacting as a system (such as a community or ecosystem).

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Thakur, M.P., van der Putten, W.H., Cobben, M.M.P. et al. Microbial invasions in terrestrial ecosystems. Nat Rev Microbiol 17, 621–631 (2019). https://doi.org/10.1038/s41579-019-0236-z

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