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 inMolecular ecology Vol. 23; no. 6; pp. 1624 - 1634
Main Authors Koch, Eric J, Miyashiro, Tim, McFall‐Ngai, Margaret J, Ruby, Edward G
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.03.2014
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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.
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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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24118200$$D View this record in MEDLINE/PubMed
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Issue 6
Keywords persistence
Vibrio fischeri
luminescence
maintenance
Euprymna scolopes
Language English
License 2013 John Wiley & Sons Ltd.
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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.
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Current address: Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802 USA
OpenAccessLink https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/mec.12474
PMID 24118200
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PublicationCentury 2000
PublicationDate March 2014
PublicationDateYYYYMMDD 2014-03-01
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  year: 2014
  text: March 2014
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
– name: Oxford
PublicationTitle Molecular ecology
PublicationTitleAlternate Mol Ecol
PublicationYear 2014
Publisher Blackwell Publishing Ltd
Publisher_xml – name: Blackwell Publishing Ltd
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2012; 61
2004; 144
2010; 77
2008; 190
1994; 176
2011; 278
2001; 183
1963; 197
2013; 27
2010; 107
2011; 82
2012; 180
2008; 9
2006; 19
1993; 184
2002; 358
2008; 6
2004; 2
2004; 306
1999; 7
1994; 60
1998; 195
2009; 11
2007; 212
2013; 15
2011; 108
2003; 425
2009; 75
2005; 102
1994; 120
2003; 8
2000; 182
2003; 69
2008; 635
2005; 7
2000; 286
2013; 110
1995; 189
2013
1997; 192
1972; 14
1998; 95
1990; 179
2012; 24
2012; 87
1991; 109
1990; 172
2009; 106
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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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SubjectTerms Aliivibrio fischeri - physiology
Animal Structures - growth & development
Animal Structures - microbiology
Animals
Decapodiformes - growth & development
Decapodiformes - microbiology
Euprymna scolopes
Light
luminescence
maintenance
Marine biology
Molecular biology
Mollusks
morphogenesis
persistence
rearing
squid
symbionts
Symbiosis
Vibrio fischeri
Title Features governing symbiont persistence in the squid–vibrio association
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https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmec.12474
https://www.ncbi.nlm.nih.gov/pubmed/24118200
https://www.proquest.com/docview/1507762886
https://search.proquest.com/docview/1508425828
https://pubmed.ncbi.nlm.nih.gov/PMC3907463
Volume 23
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