Persistent Interactions with Bacterial Symbionts Direct Mature-Host Cell Morphology and Gene Expression in the Squid-Vibrio Symbiosis

Kremer, Natacha; Koch, Eric J.; Filali, Adil El; Zhou, Lawrence; Heath‐Heckman, Elizabeth A. C.; Ruby, Edward G.; McFall‐Ngai, Margaret J.

doi:10.1128/msystems.00165-18

Cited by 17 publications

(13 citation statements)

References 61 publications

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“…S1 and Dataset S1). The large number of assembled transcripts is a common trait found in other de novo assembled transcriptomes of E. scolopes (43,44). Cephalopods are known to expand certain gene families (45,46).…”

Section: Resources For Analyses Of Symbiosis Effects On Host Gene Expmentioning

confidence: 99%

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Moriano‐Gutierrez

Koch

Bussan

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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The colonization of an animal's tissues by its microbial partners creates networks of communication across the host's body. We used the natural binary light-organ symbiosis between the squid Euprymna scolopes and its luminous bacterial partner, Vibrio fischeri, to define the impact of colonization on transcriptomic networks in the host. A night-active predator, E. scolopes coordinates the bioluminescence of its symbiont with visual cues from the environment to camouflage against moon and starlight. Like mammals, this symbiosis has a complex developmental program and a strong day/night rhythm. We determined how symbiont colonization impacted gene expression in the light organ itself, as well as in two anatomically remote organs: the eye and gill. While the overall transcriptional signature of light organ and gill were more alike, the impact of symbiosis was most pronounced and similar in light organ and eye, both in juvenile and adult animals. Furthermore, the presence of a symbiosis drove daily rhythms of transcription within all three organs. Finally, a single mutation in V. fischeri-specifically, deletion of the lux operon, which abrogates symbiont luminescence-reduced the symbiosis-dependent transcriptome of the light organ by two-thirds. In addition, while the gills responded similarly to light-organ colonization by either the wildtype or mutant, luminescence was required for all of the colonizationassociated transcriptional responses in the juvenile eye. This study defines not only the impact of symbiont colonization on the coordination of animal transcriptomes, but also provides insight into how such changes might impact the behavior and ecology of the host. squid-vibrio | symbiosis | development | daily rhythm | bioluminescence

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Section: Resources For Analyses Of Symbiosis Effects On Host Gene Expmentioning

confidence: 99%

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Moriano‐Gutierrez

Koch

Bussan

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Non-obligate two-partner systems have allowed for detailed examinations of how symbiotic partners may direct development in one another. Recent work in the Vibrio-Euprymna squid symbiosis has examined the role the bacterial symbiont V. fischeri plays in directing and maintaining "mature" morphology in the light organ of the squid [1]. Persistent colonization of the bacterial symbiont is required to efficiently regress surface epithelia and maintain the mature interior organ cell types [1].…”

Section: Introductionmentioning

confidence: 99%

“…Recent work in the Vibrio-Euprymna squid symbiosis has examined the role the bacterial symbiont V. fischeri plays in directing and maintaining "mature" morphology in the light organ of the squid [1]. Persistent colonization of the bacterial symbiont is required to efficiently regress surface epithelia and maintain the mature interior organ cell types [1]. Another prominent model for symbiont-directed host morphogenesis can also be found in the Rhizobia-legume symbiosis (as reviewed by Gage 2004) [2].…”

Section: Introductionmentioning

confidence: 99%

Micro-computed tomography permits enhanced visualization of mycangia across development and between sexes in Euwallacea ambrosia beetles

2020

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Symbiosis can facilitate the development of specialized organs in the host body to maintain relationships with beneficial microorganisms. To understand the developmental and genetic mechanisms by which such organs develop, it is critical to first investigate the morphology and developmental timing of these structures during the onset of host development. We utilized micro-computed tomography (μCT) to describe the morphology and development of mycangia, a specialized organ, in the Asian ambrosia beetle species Euwallacea validus which maintains a mutualistic relationship with the Ascomycete fungus, Fusarium oligoseptatum. We scanned animals in larval, pupal and adult life stages and identified that mycangia develop during the late pupal stage. Here we reconcile preliminary evidence and provide additional morphological data for a second paired set of structures, including the superior, medial mycangia and an inferior, lateral pair of pouch-like structures, in both late-stage pupae and adult female beetles. Furthermore, we report the possible development of rudimentary, or partially developed pairs of medial mycangia in adult male beetles which has never been reported for any male Xyleborini. Our results illustrate the validity of μCT in observing soft tissues and the complex nature of mycangia morphology and development.

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“…Interestingly, V. fischeri-induced tissue differentiation does not end there. In the adult squid, bacterial interactions with genes involved in squid retinal regeneration mediate daily changes in light organ epithelial microvilli density (Heath-Heckman et al 2016;Kremer et al 2018).…”

Section: B Symbiont Co-option Of Host Signalling Pathways and Transmentioning

confidence: 99%

Trends in symbiont-induced host cellular differentiation

Russell¹,

Castillo²

2020

Preprint

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Bacteria participate in a wide diversity of symbiotic associations with eukaryotic hosts that require precise interactions for bacterial recognition and persistence. Most commonly, host-associated bacteria interfere with host gene expression to modulate the immune response to the infection. However, many of these bacteria also interfere with host cellular differentiation pathways to create a hospitable niche, resulting in the formation of novel cell types, tissues, and organs. In both of these situations, bacterial symbionts must interact with eukaryotic regulatory pathways. Here, we detail what is known about how bacterial symbionts, from pathogens to mutualists, control host cellular differentiation across the central dogma, from epigenetic chromatin modifications, to transcription and mRNA processing, to translation and protein modifications. We identify four main trends from this survey. First, mechanisms for controlling host gene expression appear to evolve from symbionts co-opting cross-talk between host signalling pathways. Second, symbiont regulatory capacity is constrained by the processes that drive reductive genome evolution in host-associated bacteria. Third, the regulatory mechanisms symbionts exhibit correlate with the cost/benefit nature of the association. And, fourth symbiont mechanisms for interacting with host genetic regulatory elements are not bound by native bacterial capabilities. Using this knowledge, we explore how the ubiquitous intracellular Wolbachia symbiont of arthropods and nematodes may modulate host cellular differentiation to manipulate host reproduction. Our survey of the literature on how infection alters gene expression in Wolbachia and its hosts revealed that, despite their intermediate-sized genomes, different strains appear capable of a wide diversity of regulatory manipulations. Given this and Wolbachia’s diversity of phenotypes and eukaryotic-like proteins, we expect that many symbiont-induced host differentiation mechanisms will be discovered in this system.

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Persistent Interactions with Bacterial Symbionts Direct Mature-Host Cell Morphology and Gene Expression in the Squid-Vibrio Symbiosis

Cited by 17 publications

References 61 publications

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Micro-computed tomography permits enhanced visualization of mycangia across development and between sexes in Euwallacea ambrosia beetles

Trends in symbiont-induced host cellular differentiation

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