The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

McAnulty, Sarah J.; Nyholm, Spencer V.

doi:10.3389/fmicb.2016.02013

Cited by 26 publications

(22 citation statements)

References 73 publications

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“…All three of these tissues interact directly with environmental and/or symbiotic microorganisms. A number of cellular and biochemical components of the innate immune system are known to play critical roles in mediating specificity in the LO symbiosis with V. fischeri (30–32). Previous observations of host hemocytes infiltrating the ANG (7), along with expression of immune-related genes reported here, suggest that the host’s immune system plays a critical role in this symbiotic organ as well.…”

Section: Resultsmentioning

confidence: 99%

Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Belcaid

Casaburi

McAnulty

et al. 2019

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

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Microbes have been critical drivers of evolutionary innovation in animals. To understand the processes that influence the origin of specialized symbiotic organs, we report the sequencing and analysis of the genome of Euprymna scolopes, a model cephalopod with richly characterized host–microbe interactions. We identified large-scale genomic reorganization shared between E. scolopes and Octopus bimaculoides and posit that this reorganization has contributed to the evolution of cephalopod complexity. To reveal genomic signatures of host–symbiont interactions, we focused on two specialized organs of E. scolopes: the light organ, which harbors a monoculture of Vibrio fischeri, and the accessory nidamental gland (ANG), a reproductive organ containing a bacterial consortium. Our findings suggest that the two symbiotic organs within E. scolopes originated by different evolutionary mechanisms. Transcripts expressed in these microbe-associated tissues displayed their own unique signatures in both coding sequences and the surrounding regulatory regions. Compared with other tissues, the light organ showed an abundance of genes associated with immunity and mediating light, whereas the ANG was enriched in orphan genes known only from E. scolopes. Together, these analyses provide evidence for different patterns of genomic evolution of symbiotic organs within a single host.

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Section: Resultsmentioning

confidence: 99%

Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Belcaid

Casaburi

McAnulty

et al. 2019

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

Self Cite

127

189

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“…The first is a chemical signal, such as a bacterial metabolite, delivered through the circulation (63, 64); one such metabolite, acetate, is generated in the light organ as byproduct of symbiont metabolism (34). For example, the presence of V. fischeri in the light organ has a systemic effect on hemocyte signaling (65). The second mode is neural: cephalopods, in particular, produce both targeted and systemic responses via their nervous system, similar to mammals, where the vagus nerve conveys information about the gut microbiota to the brain (66).…”

Section: Symbiosis-induced Changes In Squid-host Gene Expression Showmentioning

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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“…In addition, the transcript and protein abundance of many of these immune factors, as well as protein abundance of genes involved in cytoskeletal dynamics, cell adhesion, and lysosomal function changes depending on symbiotic state of the animal (Collins, Schleicher, et al, ; Schleicher et al, ). Therefore, it is likely that these changes in gene expression and protein production underlie the molecular differences in binding and phagocytosis reported in this and previous studies (McAnulty & Nyholm, ). Our results suggest that hemocyte binding and phagocytosis behavior to V. fischeri changes during development (summarized in Figure ) and future studies should focus on characterizing PRRs during this maturation process.…”

Section: Discussionmentioning

confidence: 54%

Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis

2019

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The binary association between the squid, Euprymna scolopes, and its symbiont, Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, to V. fischeri is altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition of V. fischeri. To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis of V. fischeri and nonsymbiotic Vibrio harveyi from symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization by V. fischeri did not alter juvenile hemocyte response, these cells bound a similar number of V. fischeri and V. harveyi yet phagocytosed only V. harveyi. Our results also indicate that long‐term colonization altered the adult hemocyte response to V. fischeri but not V. harveyi. All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number of V. harveyi while hemocytes from both wild‐caught and sym‐raised adults bound significantly fewer V. fischeri, although more V. fischeri were phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of both V. fischeri and V. harveyi, although more V. harveyi cells were engulfed, suggesting that blood cells from apo‐raised adults behaved similarly to juvenile hosts. Taken together, these data suggest that persistent colonization by the light organ symbiont is required for hemocytes to differentially bind and phagocytose V. fischeri. The cellular immune system of E. scolopes likely possesses multiple mechanisms at different developmental stages to promote a specific and life‐long interaction with the symbiont.

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The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

Cited by 26 publications

References 73 publications

Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

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

Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis

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