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Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

Most eukaryotic species are colonized by a microbial community – the microbiota – that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological p...

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Autores principales: Wein, Tanita, Dagan, Tal, Fraune, Sebastian, Bosch, Thomas C. G., Reusch, Thorsten B. H., Hülter, Nils F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861309/
https://www.ncbi.nlm.nih.gov/pubmed/29593687
http://dx.doi.org/10.3389/fmicb.2018.00443
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author Wein, Tanita
Dagan, Tal
Fraune, Sebastian
Bosch, Thomas C. G.
Reusch, Thorsten B. H.
Hülter, Nils F.
author_facet Wein, Tanita
Dagan, Tal
Fraune, Sebastian
Bosch, Thomas C. G.
Reusch, Thorsten B. H.
Hülter, Nils F.
author_sort Wein, Tanita
collection PubMed
description Most eukaryotic species are colonized by a microbial community – the microbiota – that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological principles that govern microbiota assembly is lacking. Here we quantify the contribution of colonizer order, arrival time and colonization history to microbiota assembly on a host. We established the freshwater polyp Hydra vulgaris and its dominant colonizer Curvibacter as a model system that enables the visualization and quantification of colonizer population size at the single cell resolution, in vivo, in real time. We estimate the carrying capacity of a single Hydra polyp as 2 × 10(5) Curvibacter cells, which is robust among individuals and time. Colonization experiments reveal a clear priority effect of first colonizers that depends on arrival time and colonization history. First arriving colonizers achieve a numerical advantage over secondary colonizers within a short time lag of 24 h. Furthermore, colonizers primed for the Hydra habitat achieve a numerical advantage in the absence of a time lag. These results follow the theoretical expectations for any bacterial habitat with a finite carrying capacity. Thus, Hydra colonization and succession processes are largely determined by the habitat occupancy over time and Curvibacter colonization history. Our experiments provide empirical data on the basic steps of host-associated microbiota establishment – the colonization stage. The presented approach supplies a framework for studying habitat characteristics and colonization dynamics within the host–microbe setting.
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spelling pubmed-58613092018-03-28 Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat Wein, Tanita Dagan, Tal Fraune, Sebastian Bosch, Thomas C. G. Reusch, Thorsten B. H. Hülter, Nils F. Front Microbiol Microbiology Most eukaryotic species are colonized by a microbial community – the microbiota – that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological principles that govern microbiota assembly is lacking. Here we quantify the contribution of colonizer order, arrival time and colonization history to microbiota assembly on a host. We established the freshwater polyp Hydra vulgaris and its dominant colonizer Curvibacter as a model system that enables the visualization and quantification of colonizer population size at the single cell resolution, in vivo, in real time. We estimate the carrying capacity of a single Hydra polyp as 2 × 10(5) Curvibacter cells, which is robust among individuals and time. Colonization experiments reveal a clear priority effect of first colonizers that depends on arrival time and colonization history. First arriving colonizers achieve a numerical advantage over secondary colonizers within a short time lag of 24 h. Furthermore, colonizers primed for the Hydra habitat achieve a numerical advantage in the absence of a time lag. These results follow the theoretical expectations for any bacterial habitat with a finite carrying capacity. Thus, Hydra colonization and succession processes are largely determined by the habitat occupancy over time and Curvibacter colonization history. Our experiments provide empirical data on the basic steps of host-associated microbiota establishment – the colonization stage. The presented approach supplies a framework for studying habitat characteristics and colonization dynamics within the host–microbe setting. Frontiers Media S.A. 2018-03-14 /pmc/articles/PMC5861309/ /pubmed/29593687 http://dx.doi.org/10.3389/fmicb.2018.00443 Text en Copyright © 2018 Wein, Dagan, Fraune, Bosch, Reusch and Hülter. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wein, Tanita
Dagan, Tal
Fraune, Sebastian
Bosch, Thomas C. G.
Reusch, Thorsten B. H.
Hülter, Nils F.
Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title_full Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title_fullStr Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title_full_unstemmed Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title_short Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat
title_sort carrying capacity and colonization dynamics of curvibacter in the hydra host habitat
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861309/
https://www.ncbi.nlm.nih.gov/pubmed/29593687
http://dx.doi.org/10.3389/fmicb.2018.00443
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