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Title: Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

Abstract

ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions,more » were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).« less

Authors:
ORCiD logo; ; ; ORCiD logo
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1690276
Alternate Identifier(s):
OSTI ID: 1739971
Report Number(s):
LA-UR-19-27879
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
89233218CNA000001; 20180746PRD3; 2018LANLF255
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 11 Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
Country unknown/Code not available
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbiome engineering; probiotics; ecosystem manipulation; invasion biology; bacterial traits; ecosystem functioning; fungal traits; microbial composition

Citation Formats

Albright, Michaeline N., Sevanto, Sanna, Gallegos-Graves, La Verne, and Dunbar, John. Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions. Country unknown/Code not available: N. p., 2020. Web. https://doi.org/10.1128/mbio.02089-20.
Albright, Michaeline N., Sevanto, Sanna, Gallegos-Graves, La Verne, & Dunbar, John. Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions. Country unknown/Code not available. https://doi.org/10.1128/mbio.02089-20
Albright, Michaeline N., Sevanto, Sanna, Gallegos-Graves, La Verne, and Dunbar, John. Tue . "Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions". Country unknown/Code not available. https://doi.org/10.1128/mbio.02089-20.
@article{osti_1690276,
title = {Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions},
author = {Albright, Michaeline N. and Sevanto, Sanna and Gallegos-Graves, La Verne and Dunbar, John},
abstractNote = {ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).},
doi = {10.1128/mbio.02089-20},
journal = {mBio (Online)},
number = 5,
volume = 11,
place = {Country unknown/Code not available},
year = {2020},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mbio.02089-20

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