Physiological Responses to Stress in the Vibrionaceae

Soto, William; Lostroh, Phoebe; Nishiguchi, Michele K.

doi:10.1007/978-90-481-9449-0_20

Cited by 12 publications

(25 citation statements)

References 77 publications

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“…Additionally, earlier work strongly suggested variable environments and symbiosis were correlated in their effects on V. fischeri microbial growth (Soto et al 2009), providing evidence that stress on microbial physiology induced by abiotic factors and host colonization (e.g. , immune defenses) may be coupled (Soto et al 2010). How bacterial stress responses of host-associated prokaryotes react to challenges imposed by abiotic factors versus host immunity is poorly studied.…”

Section: Resultsmentioning

confidence: 99%

“…This abandonment and reacquisition of the symbiont lifestyle from an obligately free-living one has occurred numerous times based on phylogenetic analysis of closely related Vibrio species (Nishiguchi and Nair 2003). Vibrio fischeri is capable of persisting as a native part of marine sediment and sand biofilm microflora, skin and gut commensals of marine animals, and attached to floating debris, particles, zooplankton, phytoplankton, and carrion (Nishiguchi and Jones 2004; Soto et al 2010). …”

mentioning

confidence: 99%

“…V. fischeri ES114 from the Hawaiian bobtail squid ( E. scolopes ) was serially passaged through the novel host E. tasmanica , the Australian dumpling squid. The goal was to use experimental evolution to adapt nonnative symbiont V. fischeri ES114 from Hawaiian E. scolopes to Australian host E. tasmanica for 500 generations to increase the competitive ability of a derived nonnative symbiont relative to the ancestral clone (Soto et al 2010). This approach gave the nonnative symbiont a chance to become adapted to the novel host.…”

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confidence: 99%

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Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

2012

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The symbiosis between marine bioluminescent Vibrio bacteria and the sepiolid squid Euprymna is a model for studying animal–bacterial Interactions. Vibrio symbionts native to particular Euprymna species are competitively dominant, capable of outcompeting foreign Vibrio strains from other Euprymna host species. Despite competitive dominance, secondary colonization events by invading nonnative Vibrio fischeri have occurred. Competitive dominance can be offset through superior nonnative numbers and advantage of early start host colonization by nonnatives, granting nonnative vibrios an opportunity to establish beachheads in foreign Euprymna hosts. Here, we show that nonnative V. fischeri are capable of rapid adaptation to novel sepiolid squid hosts by serially passaging V. fischeri JRM200 (native to Hawaiian Euprymna scolopes) lines through the novel Australian squid host E. tasmanica for 500 generations. These experiments were complemented by a temporal population genetics survey of V. fischeri, collected from E. tasmanica over a decade, which provided a perspective from the natural history of V. fischeri evolution over 15,000–20,000 generations in E. tasmanica. No symbiont anagenic evolution within squids was observed, as competitive dominance does not purge V. fischeri genetic diversity through time. Instead, abiotic factors affecting abundance of V. fischeri variants in the planktonic phase sustain temporal symbiont diversity, a property itself of ecological constraints imposed by V. fischeri host adaptation.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

2012

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“…Bioluminescence in V. fischeri is necessary for sepiolid squid colonization, as lux null mutants display defects in colonization ability [6, 50, 51]. Negative control E. coli K12 MG1655 was never luminous.…”

Section: Resultsmentioning

confidence: 99%

Ecological Diversification of Vibrio fischeri Serially Passaged for 500 Generations in Novel Squid Host Euprymna tasmanica

2014

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Vibrio fischeri isolated from Euprymna scolopes (Cephalopoda: Sepiolidae) was used to create twenty-four lines that were serially passaged through the non-native host E. tasmanica for 500 generations. These derived lines were characterized for biofilm formation, swarming motility, carbon source utilization, and in vitro bioluminescence. Phenotypic assays were compared between “ES” (E. scolopes) and “ET” (E. tasmanica) V. fischeri wild isolates to determine if convergent evolution was apparent between E. tasmanica evolved lines and ET V. fischeri. Ecological diversification was observed in utilization of most carbon sources examined. Convergent evolution was evident in motility, biofilm formation, and select carbon sources displaying hyperpolymorphic usage in V. fischeri. Convergence in bioluminescence (a 2.5-fold increase in brightness) was collectively evident in the derived lines relative to the ancestor. However, dramatic changes in other properties—time points and cell densities of first light emission and maximal light output and emergence of a lag phase in growth curves of derived lines suggest increased light intensity per se was not the only important factor. Convergent evolution implies gnotobiotic squid light organs subject colonizing V. fischeri to similar selection pressures. Adaptation to novel hosts appears to involve flexible microbial metabolism, establishment of biofilm and swarmer V. fischeri ecotypes, and complex changes in bioluminescence. Our data demonstrate numerous alternate fitness optima or peaks are available to V. fischeri in host adaptive landscapes, where novel host squids serve as habitat islands. Thus, V. fischeri founder flushes occur during the initiation of light organ colonization that ultimately trigger founder effect diversification.

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“…Interactions such as those between symbiotic bacteria and mannose or other sugar‐containing residues are commonly found in environmentally transmitted associations (Nishiguchi et al , 2008; Nyholm & Nishiguchi, 2008), providing yet another mechanism for recognizing specific partners. This is particularly important in associations where a few bacteria are responsible for initiating the colonization of a new host amidst a number of abiotic and biotic forces that may delay or deter colonization from ever occurring (Soto et al , 2009a, b).…”

Section: Resultsmentioning

confidence: 99%

Characterization ofâ two host-specific genes, mannose-sensitive hemagglutinin (mshA) and uridyl phosphate dehydrogenase (UDPDH) that are involved in theVibrio fischeriâEuprymna tasmanicaâmutualism

Ariyakumar

Nishiguchi

2009

FEMS Microbiology Letters

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While much has been known about the mutualistic associations between the sepiolid squid Euprymna tasmanica and the luminescent bacterium, Vibrio fischeri, less is known about the connectivity between the microscopic and molecular basis of initial attachment and persistence in the light organ. Here, we examine the possible effects of two symbiotic genes on specificity and biofilm formation of V. fischeri in squid light organs. Uridine diphosphate-dehydrogenase (UDPDH) and mannose-sensitive hemagglutinin (mshA) mutants were generated in V. fischeri to determine whether each gene has an effect on host colonization, specificity, and biofilm formation. Both squid light organ colonization assays and transmission electron microscopy (TEM) confirmed differences in host colonization between wild-type and mutant strains, and also demonstrated the importance of both UDPDH and mshA gene expression for successful light organ colonization, and furthers our understanding of the genetic factors playing important roles in this environmentally transmitted symbiosis.

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Physiological Responses to Stress in the Vibrionaceae

Cited by 12 publications

References 77 publications

Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

Ecological Diversification of Vibrio fischeri Serially Passaged for 500 Generations in Novel Squid Host Euprymna tasmanica

Characterization ofâ two host-specific genes, mannose-sensitive hemagglutinin (mshA) and uridyl phosphate dehydrogenase (UDPDH) that are involved in theVibrio fischeriâEuprymna tasmanicaâmutualism

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Physiological Responses to Stress in the Vibrionaceae

Cited by 12 publications

References 77 publications

Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics

Ecological Diversification of Vibrio fischeri Serially Passaged for 500 Generations in Novel Squid Host Euprymna tasmanica

Characterization ofâ two host-specific genes, mannose-sensitive hemagglutinin (mshA) and uridyl phosphate dehydrogenase (UDPDH) that are involved in theVibrio fischeriâEuprymna tasmanicaâmutualism

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Characterization ofâ two host-specific genes, mannose-sensitive hemagglutinin (mshA) and uridyl phosphate dehydrogenase (UDPDH) that are involved in theVibrio fischeriâEuprymna tasmanicaâmutualism