Disturbance Promotes Non-Indigenous Bacterial Invasion in Soil Microcosms: Analysis of the Roles of Resource Availability and Community Structure

Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understandi...

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Published inPloS one Vol. 7; no. 10; p. e45306
Main Authors Liu, Manqiang, Bjørnlund, Lisa, Rønn, Regin, Christensen, Søren, Ekelund, Flemming
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 02.10.2012
Public Library of Science (PLoS)
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ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0045306

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Abstract Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
AbstractList Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
Background Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Methodology/Principal Findings Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. Conclusion We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life.BACKGROUNDInvasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life.Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure.METHODOLOGY/PRINCIPAL FINDINGSHere, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure.We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.CONCLUSIONWe propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
Background Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Methodology/Principal Findings Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. Conclusion We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.
Audience Academic
Author Ekelund, Flemming
Christensen, Søren
Bjørnlund, Lisa
Liu, Manqiang
Rønn, Regin
AuthorAffiliation 1 Soil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, China
2 Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Copenhagen K, Denmark
U. S. Salinity Lab, United States of America
AuthorAffiliation_xml – name: 1 Soil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, China
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– name: 2 Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Copenhagen K, Denmark
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23056198$$D View this record in MEDLINE/PubMed
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Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Conceived and designed the experiments: ML LB RR SC FE. Performed the experiments: ML LB RR SC FE. Analyzed the data: ML LB RR SC FE. Contributed reagents/materials/analysis tools: ML LB RR SC FE. Wrote the paper: ML LB RR SC FE.
Competing Interests: The authors have declared that no competing interests exist.
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– reference: 15965723 - Microb Ecol. 2005 Feb;49(2):257-64
– reference: 18027767 - Ecology. 2007 Oct;88(10):2651-61
– reference: 20014589 - Ecol Appl. 2009 Dec;19(8):2210-27
– reference: 21054733 - Ecol Lett. 2010 Dec;13(12):1560-72
– reference: 28313621 - Oecologia. 1993 Mar;93(2):303-306
– reference: 18043631 - ISME J. 2007 Jul;1(3):204-14
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Snippet Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using...
Background Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By...
Background Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By...
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SubjectTerms Agriculture
Amoeba - growth & development
Analysis
Anthropogenic factors
Availability
Bacteria
Bacteria - growth & development
Biodiversity
Biology
Carbon - analysis
Carbon - metabolism
Communities
Community structure
Control stability
Disturbance
Disturbances
Ecology
Ecology - methods
Ecosystem
Ecosystem biology
Ecosystems
Environmental changes
Environmental Monitoring - methods
Experiments
Heating
Hot Temperature
Hypotheses
Microbiology
Microcosms
Population Dynamics
Predation
Pseudomonas
Pseudomonas fluorescens
Pseudomonas fluorescens - growth & development
Remediation
Resource availability
Soil - analysis
Soil bacteria
Soil Microbiology
Soil microorganisms
Soil remediation
Soils
Studies
Substrates
Success
Time Factors
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Title Disturbance Promotes Non-Indigenous Bacterial Invasion in Soil Microcosms: Analysis of the Roles of Resource Availability and Community Structure
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Volume 7
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