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Microbial invasions in terrestrial ecosystems

Abstract

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.

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Acknowledgements

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.

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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.

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Correspondence to Madhav P. Thakur.

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Nature Reviews Microbiology thanks M. Fisher and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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CAB International: https://www.cabi.org/ISC/

GRIIS database: http://www.griis.org/

Supplementary information

Glossary

Introduction

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

Spread

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

Transport

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

Establishment

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.

Microcosms

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.

Invasibility

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

Virulence

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.

Dilution

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

Evenness

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.

Networks

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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