Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>

ABSTRACT Adult Drosophila melanogaster raised in the absence of symbiotic bacteria have fewer intestinal stem cell divisions and a longer life span than their conventionally reared counterparts. However, we do not know if increased stem cell divisions are essential for symbiont-dependent regulation...

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Autores principales: David Fast, Aashna Duggal, Edan Foley
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:b3fba6b799a643fb8f282519621ca4522021-11-15T16:00:14ZMonoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>10.1128/mBio.01114-182150-7511https://doaj.org/article/b3fba6b799a643fb8f282519621ca4522018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01114-18https://doaj.org/toc/2150-7511ABSTRACT Adult Drosophila melanogaster raised in the absence of symbiotic bacteria have fewer intestinal stem cell divisions and a longer life span than their conventionally reared counterparts. However, we do not know if increased stem cell divisions are essential for symbiont-dependent regulation of longevity. To determine if individual symbionts cause aging-dependent death in Drosophila, we examined the impacts of common symbionts on host longevity. We found that monoassociation of adult Drosophila with Lactobacillus plantarum, a widely reported fly symbiont and member of the probiotic Lactobacillus genus, curtails adult longevity relative to germfree counterparts. The effects of Lactobacillus plantarum on life span were independent of intestinal aging. Instead, we found that association with Lactobacillus plantarum causes an extensive intestinal pathology within the host, characterized by loss of stem cells, impaired epithelial renewal, and a gradual erosion of epithelial ultrastructure. Our study uncovers an unknown aspect of Lactobacillus plantarum-Drosophila interactions and establishes a simple model to characterize symbiont-dependent disruption of intestinal homeostasis. IMPORTANCE Under homeostatic conditions, gut bacteria provide molecular signals that support the organization and function of the host intestine. Sudden shifts in the composition or distribution of gut bacterial communities impact host receipt of bacterial cues and disrupt tightly regulated homeostatic networks. We used the Drosophila melanogaster model to determine the effects of prominent fly symbionts on host longevity and intestinal homeostasis. We found that monoassociation with Lactobacillus plantarum leads to a loss of intestinal progenitor cells, impaired epithelial renewal, and disruption of gut architecture as flies age. These observations uncover a novel phenotype caused by monoassociation of a germfree host with a common symbiont and establish a simple model to characterize symbiont-dependent loss of intestinal homeostasis.David FastAashna DuggalEdan FoleyAmerican Society for MicrobiologyarticleDrosophilaLactobacillusepithelial cellshost responsestem cellssymbiontsMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic Drosophila
Lactobacillus
epithelial cells
host response
stem cells
symbionts
Microbiology
QR1-502
spellingShingle Drosophila
Lactobacillus
epithelial cells
host response
stem cells
symbionts
Microbiology
QR1-502
David Fast
Aashna Duggal
Edan Foley
Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
description ABSTRACT Adult Drosophila melanogaster raised in the absence of symbiotic bacteria have fewer intestinal stem cell divisions and a longer life span than their conventionally reared counterparts. However, we do not know if increased stem cell divisions are essential for symbiont-dependent regulation of longevity. To determine if individual symbionts cause aging-dependent death in Drosophila, we examined the impacts of common symbionts on host longevity. We found that monoassociation of adult Drosophila with Lactobacillus plantarum, a widely reported fly symbiont and member of the probiotic Lactobacillus genus, curtails adult longevity relative to germfree counterparts. The effects of Lactobacillus plantarum on life span were independent of intestinal aging. Instead, we found that association with Lactobacillus plantarum causes an extensive intestinal pathology within the host, characterized by loss of stem cells, impaired epithelial renewal, and a gradual erosion of epithelial ultrastructure. Our study uncovers an unknown aspect of Lactobacillus plantarum-Drosophila interactions and establishes a simple model to characterize symbiont-dependent disruption of intestinal homeostasis. IMPORTANCE Under homeostatic conditions, gut bacteria provide molecular signals that support the organization and function of the host intestine. Sudden shifts in the composition or distribution of gut bacterial communities impact host receipt of bacterial cues and disrupt tightly regulated homeostatic networks. We used the Drosophila melanogaster model to determine the effects of prominent fly symbionts on host longevity and intestinal homeostasis. We found that monoassociation with Lactobacillus plantarum leads to a loss of intestinal progenitor cells, impaired epithelial renewal, and disruption of gut architecture as flies age. These observations uncover a novel phenotype caused by monoassociation of a germfree host with a common symbiont and establish a simple model to characterize symbiont-dependent loss of intestinal homeostasis.
format article
author David Fast
Aashna Duggal
Edan Foley
author_facet David Fast
Aashna Duggal
Edan Foley
author_sort David Fast
title Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_short Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_fullStr Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full_unstemmed Monoassociation with <named-content content-type="genus-species">Lactobacillus plantarum</named-content> Disrupts Intestinal Homeostasis in Adult <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_sort monoassociation with <named-content content-type="genus-species">lactobacillus plantarum</named-content> disrupts intestinal homeostasis in adult <named-content content-type="genus-species">drosophila melanogaster</named-content>
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/b3fba6b799a643fb8f282519621ca452
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AT edanfoley monoassociationwithnamedcontentcontenttypegenusspecieslactobacillusplantarumnamedcontentdisruptsintestinalhomeostasisinadultnamedcontentcontenttypegenusspeciesdrosophilamelanogasternamedcontent
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