Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership
Abstract Background Many animals and plants acquire their coevolved symbiotic partners shortly post-embryonic development. Thus, during embryogenesis, cellular features must be developed that will promote both symbiont colonization of the appropriate tissues, as well as persistence at those sites. W...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-03-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01509-x |
| _version_ | 1797853682271780864 |
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| author | Tara Essock-Burns Susannah Lawhorn Leo Wu Sawyer McClosky Silvia Moriano-Gutierrez Edward G. Ruby Margaret J. McFall-Ngai |
| author_facet | Tara Essock-Burns Susannah Lawhorn Leo Wu Sawyer McClosky Silvia Moriano-Gutierrez Edward G. Ruby Margaret J. McFall-Ngai |
| author_sort | Tara Essock-Burns |
| collection | DOAJ |
| description | Abstract Background Many animals and plants acquire their coevolved symbiotic partners shortly post-embryonic development. Thus, during embryogenesis, cellular features must be developed that will promote both symbiont colonization of the appropriate tissues, as well as persistence at those sites. While variation in the degree of maturation occurs in newborn tissues, little is unknown about how this variation influences the establishment and persistence of host-microbe associations. Results The binary symbiosis model, the squid-vibrio (Euprymna scolopes-Vibrio fischeri) system, offers a way to study how an environmental gram-negative bacterium establishes a beneficial, persistent, extracellular colonization of an animal host. Here, we show that bacterial symbionts occupy six different colonization sites in the light-emitting organ of the host that have both distinct morphologies and responses to antibiotic treatment. Vibrio fischeri was most resilient to antibiotic disturbance when contained within the smallest and least mature colonization sites. We show that this variability in crypt development at the time of hatching allows the immature sites to act as a symbiont reservoir that has the potential to reseed the more mature sites in the host organ when they have been cleared by antibiotic treatment. This strategy may produce an ecologically significant resiliency to the association. Conclusions The data presented here provide evidence that the evolution of the squid-vibrio association has been selected for a nascent organ with a range of host tissue maturity at the onset of symbiosis. The resulting variation in physical and chemical environments results in a spectrum of host-symbiont interactions, notably, variation in susceptibility to environmental disturbance. This “insurance policy” provides resiliency to the symbiosis during the critical period of its early development. While differences in tissue maturity at birth have been documented in other animals, such as along the infant gut tract of mammals, the impact of this variation on host-microbiome interactions has not been studied. Because a wide variety of symbiosis characters are highly conserved over animal evolution, studies of the squid-vibrio association have the promise of providing insights into basic strategies that ensure successful bacterial passage between hosts in horizontally transmitted symbioses. Video Abstract |
| first_indexed | 2024-04-09T19:54:38Z |
| format | Article |
| id | doaj.art-da78970e8e7947f8bcd6f939c464e8dc |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-09T19:54:38Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-da78970e8e7947f8bcd6f939c464e8dc2023-04-03T05:34:04ZengBMCMicrobiome2049-26182023-03-0111111610.1186/s40168-023-01509-xMaturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnershipTara Essock-Burns0Susannah Lawhorn1Leo Wu2Sawyer McClosky3Silvia Moriano-Gutierrez4Edward G. Ruby5Margaret J. McFall-Ngai6Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iKewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai’iAbstract Background Many animals and plants acquire their coevolved symbiotic partners shortly post-embryonic development. Thus, during embryogenesis, cellular features must be developed that will promote both symbiont colonization of the appropriate tissues, as well as persistence at those sites. While variation in the degree of maturation occurs in newborn tissues, little is unknown about how this variation influences the establishment and persistence of host-microbe associations. Results The binary symbiosis model, the squid-vibrio (Euprymna scolopes-Vibrio fischeri) system, offers a way to study how an environmental gram-negative bacterium establishes a beneficial, persistent, extracellular colonization of an animal host. Here, we show that bacterial symbionts occupy six different colonization sites in the light-emitting organ of the host that have both distinct morphologies and responses to antibiotic treatment. Vibrio fischeri was most resilient to antibiotic disturbance when contained within the smallest and least mature colonization sites. We show that this variability in crypt development at the time of hatching allows the immature sites to act as a symbiont reservoir that has the potential to reseed the more mature sites in the host organ when they have been cleared by antibiotic treatment. This strategy may produce an ecologically significant resiliency to the association. Conclusions The data presented here provide evidence that the evolution of the squid-vibrio association has been selected for a nascent organ with a range of host tissue maturity at the onset of symbiosis. The resulting variation in physical and chemical environments results in a spectrum of host-symbiont interactions, notably, variation in susceptibility to environmental disturbance. This “insurance policy” provides resiliency to the symbiosis during the critical period of its early development. While differences in tissue maturity at birth have been documented in other animals, such as along the infant gut tract of mammals, the impact of this variation on host-microbiome interactions has not been studied. Because a wide variety of symbiosis characters are highly conserved over animal evolution, studies of the squid-vibrio association have the promise of providing insights into basic strategies that ensure successful bacterial passage between hosts in horizontally transmitted symbioses. Video Abstracthttps://doi.org/10.1186/s40168-023-01509-xEuprymna scolopesVibrio fischeriMicrobiotaAntibioticChloramphenicolSymbiosis |
| spellingShingle | Tara Essock-Burns Susannah Lawhorn Leo Wu Sawyer McClosky Silvia Moriano-Gutierrez Edward G. Ruby Margaret J. McFall-Ngai Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership Microbiome Euprymna scolopes Vibrio fischeri Microbiota Antibiotic Chloramphenicol Symbiosis |
| title | Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership |
| title_full | Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership |
| title_fullStr | Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership |
| title_full_unstemmed | Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership |
| title_short | Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership |
| title_sort | maturation state of colonization sites promotes symbiotic resiliency in the euprymna scolopes vibrio fischeri partnership |
| topic | Euprymna scolopes Vibrio fischeri Microbiota Antibiotic Chloramphenicol Symbiosis |
| url | https://doi.org/10.1186/s40168-023-01509-x |
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