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Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession
A large number of descriptive surveys have shown that microbial communities experience successional changes over time and that ecological dominance is common in the microbial world. However, direct evidence for the ecological processes mediating succession or causing ecological dominance remains rar...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414377/ https://www.ncbi.nlm.nih.gov/pubmed/30635382 http://dx.doi.org/10.1128/AEM.02421-18 |
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author | Boynton, Primrose J. Peterson, Celeste N. Pringle, Anne |
author_facet | Boynton, Primrose J. Peterson, Celeste N. Pringle, Anne |
author_sort | Boynton, Primrose J. |
collection | PubMed |
description | A large number of descriptive surveys have shown that microbial communities experience successional changes over time and that ecological dominance is common in the microbial world. However, direct evidence for the ecological processes mediating succession or causing ecological dominance remains rare. Different dispersal abilities among species may be a key mechanism. We surveyed fungal diversity within a metacommunity of pitchers of the model carnivorous plant Sarracenia purpurea and discovered that the yeast Candida pseudoglaebosa was ecologically dominant. Its frequency in the metacommunity increased during the growing season, and it was not replaced by other taxa. We next measured its competitive ability in a manipulative laboratory experiment and tracked its dispersal over time in nature. Despite its dominance, C. pseudoglaebosa is not a superior competitor. Instead, it is a superior disperser: it arrives in pitchers earlier, and disperses into more pitchers, than other fungi. Differential dispersal across the spatially structured metacommunity of individual pitchers emerges as a key driver of the continuous dominance of C. pseudoglaebosa during succession. IMPORTANCE Microbial communities are ubiquitous and occupy nearly every imaginable habitat and resource, including human-influenced habitats (e.g., fermenting food and hospital surfaces) and habitats with little human influence (e.g., aquatic communities living in carnivorous plant pitchers). We studied yeast communities living in pitchers of the carnivorous purple pitcher plant to understand how and why microbial communities change over time. We found that dispersal ability is not only important for fungal communities early in their existence, it can also determine which species is dominant (here, the yeast Candida pseudoglaebosa) long after the species and its competitors have arrived. These results contrast with observations from many human-influenced habitats, in which a good competitor eventually outcompetes good dispersers, since humans often design these habitats to favor a specific competitor. This study will help microbiologists understand the qualities of microbial species that enable takeover of new habitats in both natural and human-influenced environments. |
format | Online Article Text |
id | pubmed-6414377 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-64143772019-04-12 Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession Boynton, Primrose J. Peterson, Celeste N. Pringle, Anne Appl Environ Microbiol Microbial Ecology A large number of descriptive surveys have shown that microbial communities experience successional changes over time and that ecological dominance is common in the microbial world. However, direct evidence for the ecological processes mediating succession or causing ecological dominance remains rare. Different dispersal abilities among species may be a key mechanism. We surveyed fungal diversity within a metacommunity of pitchers of the model carnivorous plant Sarracenia purpurea and discovered that the yeast Candida pseudoglaebosa was ecologically dominant. Its frequency in the metacommunity increased during the growing season, and it was not replaced by other taxa. We next measured its competitive ability in a manipulative laboratory experiment and tracked its dispersal over time in nature. Despite its dominance, C. pseudoglaebosa is not a superior competitor. Instead, it is a superior disperser: it arrives in pitchers earlier, and disperses into more pitchers, than other fungi. Differential dispersal across the spatially structured metacommunity of individual pitchers emerges as a key driver of the continuous dominance of C. pseudoglaebosa during succession. IMPORTANCE Microbial communities are ubiquitous and occupy nearly every imaginable habitat and resource, including human-influenced habitats (e.g., fermenting food and hospital surfaces) and habitats with little human influence (e.g., aquatic communities living in carnivorous plant pitchers). We studied yeast communities living in pitchers of the carnivorous purple pitcher plant to understand how and why microbial communities change over time. We found that dispersal ability is not only important for fungal communities early in their existence, it can also determine which species is dominant (here, the yeast Candida pseudoglaebosa) long after the species and its competitors have arrived. These results contrast with observations from many human-influenced habitats, in which a good competitor eventually outcompetes good dispersers, since humans often design these habitats to favor a specific competitor. This study will help microbiologists understand the qualities of microbial species that enable takeover of new habitats in both natural and human-influenced environments. American Society for Microbiology 2019-03-06 /pmc/articles/PMC6414377/ /pubmed/30635382 http://dx.doi.org/10.1128/AEM.02421-18 Text en Copyright © 2019 Boynton et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Microbial Ecology Boynton, Primrose J. Peterson, Celeste N. Pringle, Anne Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title | Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title_full | Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title_fullStr | Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title_full_unstemmed | Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title_short | Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession |
title_sort | superior dispersal ability can lead to persistent ecological dominance throughout succession |
topic | Microbial Ecology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414377/ https://www.ncbi.nlm.nih.gov/pubmed/30635382 http://dx.doi.org/10.1128/AEM.02421-18 |
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