Cargando…
Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish
BACKGROUND: Across taxa, animals with depleted intestinal microbiomes show disrupted behavioral phenotypes. Axenic (i.e., microbe-free) mice, zebrafish, and fruit flies exhibit increased locomotor behavior, or hyperactivity. The mechanism through which bacteria interact with host cells to trigger no...
Autores principales: | , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7818562/ https://www.ncbi.nlm.nih.gov/pubmed/33499997 http://dx.doi.org/10.1186/s42523-020-00069-x |
_version_ | 1783638861516111872 |
---|---|
author | Weitekamp, Chelsea A. Kvasnicka, Allison Keely, Scott P. Brinkman, Nichole E. Howey, Xia Meng Gaballah, Shaza Phelps, Drake Catron, Tara Zurlinden, Todd Wheaton, Emily Tal, Tamara |
author_facet | Weitekamp, Chelsea A. Kvasnicka, Allison Keely, Scott P. Brinkman, Nichole E. Howey, Xia Meng Gaballah, Shaza Phelps, Drake Catron, Tara Zurlinden, Todd Wheaton, Emily Tal, Tamara |
author_sort | Weitekamp, Chelsea A. |
collection | PubMed |
description | BACKGROUND: Across taxa, animals with depleted intestinal microbiomes show disrupted behavioral phenotypes. Axenic (i.e., microbe-free) mice, zebrafish, and fruit flies exhibit increased locomotor behavior, or hyperactivity. The mechanism through which bacteria interact with host cells to trigger normal neurobehavioral development in larval zebrafish is not well understood. Here, we monoassociated zebrafish with either one of six different zebrafish-associated bacteria, mixtures of these host-associates, or with an environmental bacterial isolate. RESULTS: As predicted, the axenic cohort was hyperactive. Monoassociation with three different host-associated bacterial species, as well as with the mixtures, resulted in control-like locomotor behavior. Monoassociation with one host-associate and the environmental isolate resulted in the hyperactive phenotype characteristic of axenic larvae, while monoassociation with two other host-associated bacteria partially blocked this phenotype. Furthermore, we found an inverse relationship between the total concentration of bacteria per larvae and locomotor behavior. Lastly, in the axenic and associated cohorts, but not in the larvae with complex communities, we detected unexpected bacteria, some of which may be present as facultative predators. CONCLUSIONS: These data support a growing body of evidence that individual species of bacteria can have different effects on host behavior, potentially related to their success at intestinal colonization. Specific to the zebrafish model, our results suggest that differences in the composition of microbes in fish facilities could affect the results of behavioral assays within pharmacological and toxicological studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-020-00069-x. |
format | Online Article Text |
id | pubmed-7818562 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-78185622021-01-26 Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish Weitekamp, Chelsea A. Kvasnicka, Allison Keely, Scott P. Brinkman, Nichole E. Howey, Xia Meng Gaballah, Shaza Phelps, Drake Catron, Tara Zurlinden, Todd Wheaton, Emily Tal, Tamara Anim Microbiome Research Article BACKGROUND: Across taxa, animals with depleted intestinal microbiomes show disrupted behavioral phenotypes. Axenic (i.e., microbe-free) mice, zebrafish, and fruit flies exhibit increased locomotor behavior, or hyperactivity. The mechanism through which bacteria interact with host cells to trigger normal neurobehavioral development in larval zebrafish is not well understood. Here, we monoassociated zebrafish with either one of six different zebrafish-associated bacteria, mixtures of these host-associates, or with an environmental bacterial isolate. RESULTS: As predicted, the axenic cohort was hyperactive. Monoassociation with three different host-associated bacterial species, as well as with the mixtures, resulted in control-like locomotor behavior. Monoassociation with one host-associate and the environmental isolate resulted in the hyperactive phenotype characteristic of axenic larvae, while monoassociation with two other host-associated bacteria partially blocked this phenotype. Furthermore, we found an inverse relationship between the total concentration of bacteria per larvae and locomotor behavior. Lastly, in the axenic and associated cohorts, but not in the larvae with complex communities, we detected unexpected bacteria, some of which may be present as facultative predators. CONCLUSIONS: These data support a growing body of evidence that individual species of bacteria can have different effects on host behavior, potentially related to their success at intestinal colonization. Specific to the zebrafish model, our results suggest that differences in the composition of microbes in fish facilities could affect the results of behavioral assays within pharmacological and toxicological studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-020-00069-x. BioMed Central 2021-01-21 /pmc/articles/PMC7818562/ /pubmed/33499997 http://dx.doi.org/10.1186/s42523-020-00069-x Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Research Article Weitekamp, Chelsea A. Kvasnicka, Allison Keely, Scott P. Brinkman, Nichole E. Howey, Xia Meng Gaballah, Shaza Phelps, Drake Catron, Tara Zurlinden, Todd Wheaton, Emily Tal, Tamara Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title | Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title_full | Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title_fullStr | Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title_full_unstemmed | Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title_short | Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
title_sort | monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7818562/ https://www.ncbi.nlm.nih.gov/pubmed/33499997 http://dx.doi.org/10.1186/s42523-020-00069-x |
work_keys_str_mv | AT weitekampchelseaa monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT kvasnickaallison monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT keelyscottp monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT brinkmannicholee monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT howeyxiameng monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT gaballahshaza monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT phelpsdrake monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT catrontara monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT zurlindentodd monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT wheatonemily monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish AT taltamara monoassociationwithbacterialisolatesrevealstheroleofcolonizationcommunitycomplexityandabundanceonlocomotorbehaviorinlarvalzebrafish |