Independent host- and bacterium-based determinants protect a model symbiosis from phage predation

Lynch, Jonathan B.; Bennett, Brittany D.; Merrill, Bryan D.; Ruby, Edward G.; Hryckowian, Andrew J.

doi:10.1016/j.celrep.2022.110376

Cited by 13 publications

(7 citation statements)

References 86 publications

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“…The other exopolysaccharide locus spans VF_0157-VF_0180 and is regulated by the quorum sensing regulator LitR ( 40 ). To date, the function of this locus remains unclear, yet it does appear to enhance phage infection by the V. fischeri phage HNL01 ( 6 ). In contrast to the upregulation of the bcs and syp loci within the core biofilm regulon, we noted that a majority of genes in the VF_0157-VF_0180 EPS locus were downregulated modestly in both models (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In animal-microbe mutualisms, symbionts can provide nutritional, developmental, and/or defensive benefits to the host, and in turn, the symbionts may gain various benefits from association with the host ( 1 – 6 ). During horizontal transmission, hosts must reacquire their symbionts each generation from environmental symbiont populations ( 7 – 14 ).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Vander Griend,

Isenberg,

Kotla

et al. 2024

mSystems

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Beneficial microbial symbionts that are horizontally acquired by their animal hosts undergo a lifestyle transition from free-living in the environment to associating with host tissues. In the model symbiosis between the Hawaiian bobtail squid and its microbial symbiont Vibrio fischeri , one mechanism used to make this transition during host colonization is the formation of biofilm-like aggregates in host mucosa. Previous work identified factors that are sufficient to induce V. fischeri biofilm formation, yet much remains unknown regarding the breadth of target genes induced by these factors. Here, we probed two widely used in vitro models of biofilm formation to identify novel regulatory pathways in the squid symbiont V. fischeri ES114. We discovered a shared set of 232 genes that demonstrated similar patterns in expression in both models. These genes comprise multiple exopolysaccharide loci that are upregulated and flagellar motility genes that are downregulated, with a consistent decrease in measured swimming motility. Furthermore, we identified genes regulated downstream of the key sensor kinase RscS that are induced independent of the response regulator SypG. Our data suggest that transcriptional regulator VpsR plays a strong role in expression of at least a subset of these genes. Overall, this study adds to our understanding of the genes involved in V. fischeri biofilm regulation while revealing new regulatory pathways branching from previously characterized signaling networks. IMPORTANCE The V. fischeri- squid system provides an opportunity to study biofilm development both in the animal host and in culture-based biofilm models that capture key aspects of in vivo signaling. In this work, we report the results of the transcriptomic profiling of two V. fischeri biofilm models followed by phenotypic validation and examination of novel signaling pathway architecture. Remarkable consistency between the models provides a strong basis for future studies using either approach or both. A subset of the factors identified by the approaches were validated in the work, and the body of transcriptomic data provides a number of leads for future studies in culture and during animal colonization.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Vander Griend,

Isenberg,

Kotla

et al. 2024

mSystems

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“…The overall impact of prophages on host colonization may be obscured, in part, by the influence of host genetics as suggested by differential retention rates across Ciona from different genetic backgrounds ( Figure 4 ). Of note, it was recently reported that the marine lytic phage, HLN01, has no apparent influence on how the bacterial symbiont, Vibrio fischeri , colonizes its natural host, the bobtail squid Euprymna scolopes [89].…”

Section: Discussionmentioning

confidence: 99%

Prophages regulateShewanella fidelis3313 motility and biofilm formation: implications for gut colonization dynamics inCiona robusta

Natarajan

Gibboney

Young

et al. 2022

Preprint

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Prophages are viruses that integrate into the genomes of bacteria, which then become lysogens. Lysogens are abundant in the gut of animals, where prophages are known to influence their metabolic pathways and other traits. However, the potential influence of prophages on the gut microbiota-host immune axis in animals remains poorly understood. Here, we investigated the influence of prophages in a marine lysogen,Shewanella fidelis3313, a prevalent member of the gut microbiome of the model tunicate,Ciona robusta. Two prophages, SfPat and SfMu1, were deleted individually and in combination using homologous recombination to observe the effects of these prophages on processes involved in gut colonization. We report here that in vitro, these prophages enhance motility and negatively impact biofilm formation ofS. fidelis 3313. To understand the in vivo impact of these prophage-induced changes in bacterial traits, we exposed metamorphic stage 4Cionajuveniles (the stage that correlates to first feeding and subsequent gut colonization) to both wildtype (WT) and modified strains ofS. fidelis 3313. When colonizing theCionagut, the WT strain experiences an upregulation ofpdeB, a phosphodiesterase known to degrade cyclic di-GMP, a dinucleotide messenger that can positively influence biofilm formation while negatively regulating motility. WT colonization and upregulation ofpdeBalso correlates to a downregulation of theCionagut immune effector, VCBP-C. This study reveals an influence of prophages on bacterial traits and host immune response in the gut of a model organism. Our findings highlight the importance of interkingdom signaling between prophages, bacteria, and their animal hosts in regulating the gut microbiota-host immune axis.

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“…Interestingly, resistance seems to minimally impact the bacterial ability to colonise different eukaryotic hosts under virulent phage predation, as shown by recent studies using Pseudomonas syringae infecting tomato leaves, and bobtail squid symbiont Vibrio fischeri (Hernandez and Koskella, 2019;Lynch et al, 2022). Yet, all these studies share the rapid evolution of bacterial resistance during free, planktonic, lifestyle.…”

Section: Phage-bacteria Interactions In the Intestinal Environmentmentioning

confidence: 99%

Gut bacteriophages and the pinball challenge

Sordi¹

2022

Cell Host & Microbe

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Independent host- and bacterium-based determinants protect a model symbiosis from phage predation

Cited by 13 publications

References 86 publications

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Prophages regulateShewanella fidelis3313 motility and biofilm formation: implications for gut colonization dynamics inCiona robusta

Gut bacteriophages and the pinball challenge

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