Features governing symbiont persistence in the squid–vibrio association
Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont ligh...
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Published in | Molecular ecology Vol. 23; no. 6; pp. 1624 - 1634 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
England
Blackwell Publishing Ltd
01.03.2014
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Subjects | |
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Abstract | Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late‐stage development (e.g. symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri. During the first 4 weeks postinoculation of juvenile squid, the population of wild‐type V. fischeri increased 100‐fold; in contrast, a strain defective in light production (Δlux) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co‐colonization of organs by both strains affected neither the trajectory of colonization by wild type nor the decline of Δlux levels. Uninfected animals retained the ability to be colonized for at least 2 weeks posthatch. However, once colonized by the wild‐type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host's entry into a refractory state. However, animals colonized by the Δlux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild‐type or a Δlux strain revealed slight, if any, differences in the developmental regression of the ciliated light‐organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δlux strain's defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. |
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AbstractList | Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late‐stage development (e.g. symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri. During the first 4 weeks postinoculation of juvenile squid, the population of wild‐type V. fischeri increased 100‐fold; in contrast, a strain defective in light production (Δlux) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co‐colonization of organs by both strains affected neither the trajectory of colonization by wild type nor the decline of Δlux levels. Uninfected animals retained the ability to be colonized for at least 2 weeks posthatch. However, once colonized by the wild‐type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host's entry into a refractory state. However, animals colonized by the Δlux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild‐type or a Δlux strain revealed slight, if any, differences in the developmental regression of the ciliated light‐organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δlux strain's defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late‐stage development (e.g. symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri. During the first 4 weeks postinoculation of juvenile squid, the population of wild‐type V. fischeri increased 100‐fold; in contrast, a strain defective in light production (Δlux) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co‐colonization of organs by both strains affected neither the trajectory of colonization by wild type nor the decline of Δlux levels. Uninfected animals retained the ability to be colonized for at least 2 weeks posthatch. However, once colonized by the wild‐type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host's entry into a refractory state. However, animals colonized by the Δlux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild‐type or a Δlux strain revealed slight, if any, differences in the developmental regression of the ciliated light‐organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δlux strain's defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal-bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late-stage development (e.g. symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri. During the first 4 weeks postinoculation of juvenile squid, the population of wild-type V. fischeri increased 100-fold; in contrast, a strain defective in light production ([Delta]lux) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co-colonization of organs by both strains affected neither the trajectory of colonization by wild type nor the decline of [Delta]lux levels. Uninfected animals retained the ability to be colonized for at least 2 weeks posthatch. However, once colonized by the wild-type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host's entry into a refractory state. However, animals colonized by the [Delta]lux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild-type or a [Delta]lux strain revealed slight, if any, differences in the developmental regression of the ciliated light-organ tissues that facilitate the colonization process. Thus, some other feature(s) of the [Delta]lux strain's defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. [PUBLICATION ABSTRACT] Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal-bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late-stage development ( e.g ., symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri . During the first four weeks post-inoculation of juvenile squid, the population of wild-type V. fischeri increased 100-fold; in contrast, a strain defective in light production (Δ lux ) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co-colonization of organs by both strains affected neither the trajectory of colonization by wild type, nor the decline of Δ lux levels. Uninfected animals retained the ability to be colonized for at least two weeks post-hatch. However, once colonized by the wild-type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host’s entry into a refractory state. However, animals colonized by the Δ lux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild-type or a Δ lux strain revealed slight, if any, differences in the developmental regression of the ciliated light-organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δ lux strain’s defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. Abstract Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late‐stage development ( e.g . symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri . During the first 4 weeks postinoculation of juvenile squid, the population of wild‐type V. fischeri increased 100‐fold; in contrast, a strain defective in light production (Δ lux ) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co‐colonization of organs by both strains affected neither the trajectory of colonization by wild type nor the decline of Δ lux levels. Uninfected animals retained the ability to be colonized for at least 2 weeks posthatch. However, once colonized by the wild‐type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host's entry into a refractory state. However, animals colonized by the Δ lux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild‐type or a Δ lux strain revealed slight, if any, differences in the developmental regression of the ciliated light‐organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δ lux strain's defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host. |
Author | Ruby, Edward G Miyashiro, Tim McFall‐Ngai, Margaret J Koch, Eric J |
AuthorAffiliation | Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin 53706 USA |
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Author_xml | – sequence: 1 fullname: Koch, Eric J – sequence: 2 fullname: Miyashiro, Tim – sequence: 3 fullname: McFall‐Ngai, Margaret J – sequence: 4 fullname: Ruby, Edward G |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24118200$$D View this record in MEDLINE/PubMed |
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Keywords | persistence Vibrio fischeri luminescence maintenance Euprymna scolopes |
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Notes | http://dx.doi.org/10.1111/mec.12474 NIH K99 - No. GM097032 Table S1 Progression of the E. scolopes feeding protocol during juvenile development.Fig. S1 Relative persistence of the ∆luxCDABEG during either single- (closed) or co- (open) colonization experiments over the first 14 days post-inoculation (n = 10-30 squid per time point). Each symbol indicates the number of ∆luxCDABEG CFU in an animal's light organ at different time points in a single experiment. The lines indicating the trajectory of single- (solid) and co- (dashed) colonization levels represent a nonlinear regression analysis of the decrease in ∆luxCDABEG populations for each experimental group. A statistical comparison of the kinetics of decrease indicated that they were not significantly different (P = 0.11, single-R² = 0.63, and co-R² = 0.54).Fig. S2 Comparison of growth kinetics of marked and unmarked, wild-type and ∆lux strains. Each symbol represents an average of two OD600 measurements from two experiments where each strain was grown separately in SWT medium; wild type (diamond), TIM302 (circle), TIM 313 (square), TIM386 (triangle), and TIM387 (inverted triangle).Appendix S1 Additional culturing information.Appendix S2 Single-strain colonization data of E. scolopes animals by wild type or ∆luxCDABEG V. fischeri over 4 weeks.Appendix S3 Co-colonization data of E. scolopes animals by both wild type and ∆luxCDABEG V. fischeri over 15 days. NSF - No. IOS 0817232 istex:2FB78E3FF12279B1B93E21CAD4E9ABC333BC7AD1 ArticleID:MEC12474 NIH R01 - No. AI50661; No. GM099507; No. OD11024 ark:/67375/WNG-G4HQT5QQ-8 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802 USA |
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Snippet | Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial... Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal-bacterial... Abstract Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal–bacterial... |
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Title | Features governing symbiont persistence in the squid–vibrio association |
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