Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems

ABSTRACT Animal-microbe symbioses are ubiquitous in nature and scientifically important in diverse areas, including ecology, medicine, and agriculture. Steinernema nematodes and Xenorhabdus bacteria compose an established, successful model system for investigating microbial pathogenesis and mutualis...

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Autores principales: Matthew D. Stilwell, Mengyi Cao, Heidi Goodrich-Blair, Douglas B. Weibel
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:8e93acfdf6984c6fa06c7771b85b234e2021-11-15T15:22:01ZStudying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems10.1128/mSphere.00530-172379-5042https://doaj.org/article/8e93acfdf6984c6fa06c7771b85b234e2018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00530-17https://doaj.org/toc/2379-5042ABSTRACT Animal-microbe symbioses are ubiquitous in nature and scientifically important in diverse areas, including ecology, medicine, and agriculture. Steinernema nematodes and Xenorhabdus bacteria compose an established, successful model system for investigating microbial pathogenesis and mutualism. The bacterium Xenorhabdus nematophila is a species-specific mutualist of insect-infecting Steinernema carpocapsae nematodes. The bacterium colonizes a specialized intestinal pocket within the infective stage of the nematode, which transports the bacteria between insects that are killed and consumed by the pair for reproduction. Current understanding of the interaction between the infective-stage nematode and its bacterial colonizers is based largely on population-level, snapshot time point studies on these organisms. This limitation arises because investigating temporal dynamics of the bacterium within the nematode is impeded by the difficulty of isolating and maintaining individual living nematodes and tracking colonizing bacterial cells over time. To overcome this challenge, we developed a microfluidic system that enables us to spatially isolate and microscopically observe individual, living Steinernema nematodes and monitor the growth and development of the associated X. nematophila bacterial communities—starting from a single cell or a few cells—over weeks. Our data demonstrate, to our knowledge, the first direct, temporal, in vivo visual analysis of a symbiosis system and the application of this system to reveal continuous dynamics of the symbiont population in the living host animal. IMPORTANCE This paper describes an experimental system for directly investigating population dynamics of a symbiotic bacterium, Xenorhabdus nematophila, in its host—the infective stage of the entomopathogenic nematode Steinernema carpocapsae. Tracking individual and groups of bacteria in individual host nematodes over days and weeks yielded insight into dynamic growth and topology changes of symbiotic bacterial populations within infective juvenile nematodes. Our approach for studying symbioses between bacteria and nematodes provides a system to investigate long-term host-microbe interactions in individual nematodes and extrapolate the lessons learned to other bacterium-animal interactions.Matthew D. StilwellMengyi CaoHeidi Goodrich-BlairDouglas B. WeibelAmerican Society for MicrobiologyarticleSteinernema nematodesXenorhabdus nematophilabacterial single-cell analysishost-microbe interactionsmicrofluidicsmutualismMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution DOAJ
collection DOAJ
language EN
topic Steinernema nematodes
Xenorhabdus nematophila
bacterial single-cell analysis
host-microbe interactions
microfluidics
mutualism
Microbiology
QR1-502
spellingShingle Steinernema nematodes
Xenorhabdus nematophila
bacterial single-cell analysis
host-microbe interactions
microfluidics
mutualism
Microbiology
QR1-502
Matthew D. Stilwell
Mengyi Cao
Heidi Goodrich-Blair
Douglas B. Weibel
Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
description ABSTRACT Animal-microbe symbioses are ubiquitous in nature and scientifically important in diverse areas, including ecology, medicine, and agriculture. Steinernema nematodes and Xenorhabdus bacteria compose an established, successful model system for investigating microbial pathogenesis and mutualism. The bacterium Xenorhabdus nematophila is a species-specific mutualist of insect-infecting Steinernema carpocapsae nematodes. The bacterium colonizes a specialized intestinal pocket within the infective stage of the nematode, which transports the bacteria between insects that are killed and consumed by the pair for reproduction. Current understanding of the interaction between the infective-stage nematode and its bacterial colonizers is based largely on population-level, snapshot time point studies on these organisms. This limitation arises because investigating temporal dynamics of the bacterium within the nematode is impeded by the difficulty of isolating and maintaining individual living nematodes and tracking colonizing bacterial cells over time. To overcome this challenge, we developed a microfluidic system that enables us to spatially isolate and microscopically observe individual, living Steinernema nematodes and monitor the growth and development of the associated X. nematophila bacterial communities—starting from a single cell or a few cells—over weeks. Our data demonstrate, to our knowledge, the first direct, temporal, in vivo visual analysis of a symbiosis system and the application of this system to reveal continuous dynamics of the symbiont population in the living host animal. IMPORTANCE This paper describes an experimental system for directly investigating population dynamics of a symbiotic bacterium, Xenorhabdus nematophila, in its host—the infective stage of the entomopathogenic nematode Steinernema carpocapsae. Tracking individual and groups of bacteria in individual host nematodes over days and weeks yielded insight into dynamic growth and topology changes of symbiotic bacterial populations within infective juvenile nematodes. Our approach for studying symbioses between bacteria and nematodes provides a system to investigate long-term host-microbe interactions in individual nematodes and extrapolate the lessons learned to other bacterium-animal interactions.
format article
author Matthew D. Stilwell
Mengyi Cao
Heidi Goodrich-Blair
Douglas B. Weibel
author_facet Matthew D. Stilwell
Mengyi Cao
Heidi Goodrich-Blair
Douglas B. Weibel
author_sort Matthew D. Stilwell
title Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
title_short Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
title_full Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
title_fullStr Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
title_full_unstemmed Studying the Symbiotic Bacterium <named-content content-type="genus-species">Xenorhabdus nematophila</named-content> in Individual, Living <italic toggle="yes">Steinernema carpocapsae</italic> Nematodes Using Microfluidic Systems
title_sort studying the symbiotic bacterium <named-content content-type="genus-species">xenorhabdus nematophila</named-content> in individual, living <italic toggle="yes">steinernema carpocapsae</italic> nematodes using microfluidic systems
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/8e93acfdf6984c6fa06c7771b85b234e
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