Immune activity at the gut epithelium in the larval sea urchin

Buckley, Katherine M.; Rast, Jonathan P.

doi:10.1007/s00441-019-03095-7

Cited by 28 publications

(19 citation statements)

References 37 publications

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“…Upon dissection of these animals, no morphological abnormalities were seen (data not shown). Because of the link between echinochrome pigment and immune defense 31 , we surmise that the albino animals succumbed to a microbe(s) for which pigmented animals (wild-type and other targeted gene Cas9-gRNA animals) were otherwise immune. www.nature.com/scientificreports www.nature.com/scientificreports/ Mosaicism of pigmentation was seen in several of the GCM-KO and PKS-KO animals (Fig.…”

Section: Resultsmentioning

confidence: 99%

Genetic manipulation of the pigment pathway in a sea urchin reveals distinct lineage commitment prior to metamorphosis in the bilateral to radial body plan transition

Wessel

Kiyomoto

Shen

et al. 2020

Sci Rep

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echinoderms display a vast array of pigmentation and patterning in larval and adult life stages. this coloration is thought to be important for immune defense and camouflage. However, neither the cellular nor molecular mechanism that regulates this complex coloration in the adult is known. Here we knocked out three different genes thought to be involved in the pigmentation pathway(s) of larvae and grew the embryos to adulthood. The genes tested were polyketide synthase (PKS), Flavindependent monooxygenase family 3 (FMO3) and glial cells missing (GCM). We found that disabling of the pKS gene at fertilization resulted in albinism throughout all life stages and throughout all cells and tissues of this animal, including the immune cells of the coelomocytes. We also learned that FMO3 is an essential modifier of the polyketide. FMO3 activity is essential for larval pigmentation, but in juveniles and adults, loss of FMO3 activity resulted in the animal becoming pastel purple. Linking the LC-MS analysis of this modified pigment to a naturally purple animal suggested a conserved echinochrome profile yielding a pastel purple. We interpret this result as FMO3 modifies the parent polyketide to contribute to the normal brown/green color of the animal, and that in its absence, other biochemical modifications are revealed, perhaps by other members of the large FMO family in this animal. The fMo modularity revealed here may be important in the evolutionary changes between species and for different immune challenges. We also learned that glial cells missing (GCM), a key transcription factor of the endomesoderm gene regulatory network of embryos in the sea urchin, is required for pigmentation throughout the life stages of this sea urchin, but surprisingly, is not essential for larval development, metamorphosis, or maintenance of adulthood. Mosaic knockout of either PKS or GCM revealed spatial lineage commitment in the transition from bilaterality of the larva to a pentaradial body plan of the adult. The cellular lineages identified by pigment presence or absence (wild-type or knockout lineages, respectively) followed a strict oral/aboral profile. No circumferential segments were seen and instead we observed 10-fold symmetry in the segments of pigment expression. This suggests that the adult lineage commitments in the five outgrowths of the hydropore in the larva are early, complete, fixed, and each bilaterally symmetric. Overall, these results suggest that pigmentation of this animal is genetically determined and dependent on a population of pigment stem cells that are set-aside in a subregion of each outgrowth of the pentaradial adult rudiment prior to metamorphosis. this study reveals the complex chemistry of pigment applicable to many organisms, and further, provides an insight into the key transitions from bilateral to pentaradial body plans unique to echinoderms.

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Section: Resultsmentioning

confidence: 99%

Genetic manipulation of the pigment pathway in a sea urchin reveals distinct lineage commitment prior to metamorphosis in the bilateral to radial body plan transition

Wessel

Kiyomoto

Shen

et al. 2020

Sci Rep

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“…Ho et al, 2016). At this time point, increases in the expression level of other gut-related genes including Soul1, IL-17-4 and IL-17-1 have been observed in response to a Vibrio infection, followed by a progressive decrease in expression levels over the time course of 24 h (Buckley and Rast, 2019). The relative synchrony of the cellular immune response with changes in midgut pH homeostasis after Vibrio infection suggests an orchestration of these systems in response to a bacterial infection of the gut.…”

Section: Response Of the Midgut Ph Homeostasis During Bacterial Infecmentioning

confidence: 84%

“…In fact, distinct microbial compositions were associated with different developmental stages of the sea urchin larva, with a strong decrease in bacterial diversity and abundance in larvae after the development of the functional gut (Carrier and Reitzel, 2019b). In addition, the larval gut appears to represent an important site for the coordination of a cellular immune response during bacterial infections (Buckley and Rast, 2019). These observations strongly suggest a concerted action of cellular immune responses and midgut pH in regulating the larval microbiome.…”

Section: Discussionmentioning

confidence: 96%

Alkaline guts contribute to immunity during exposure to acidified seawater in the sea urchin larva

Stumpp

Petersen

Thoben

et al. 2020

Journal of Experimental Biology

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Larval stages of members of the Abulacraria superphylum including echinoderms and hemichordates have highly alkaline midguts. To date, the reason for the evolution of such extreme pH conditions in the gut of these organisms remains unknown. Here, we test the hypothesis that, analogous to the acidic stomachs of vertebrates, these alkaline conditions may represent a first defensive barrier to protect from environmental pathogens. pH-optimum curves for five different species of marine bacteria demonstrated a rapid decrease in proliferation rates by 50-60% between pH 8.5 and 9.5. Using the marine bacterium Vibrio diazotrophicus, which elicits a coordinated immune response in the larvae of the sea urchin Strongylocentrotus purpuratus, we studied the physiological responses of the midgut pH regulatory machinery to this pathogen. Gastroscopic microelectrode measurements demonstrate a stimulation of midgut alkalization upon infection with V. diazotrophicus accompanied by an upregulation of acid-base transporter transcripts of the midgut. Pharmacological inhibition of midgut alkalization resulted in an increased mortality rate of larvae during Vibrio infection. Reductions in seawater pH resembling ocean acidification conditions lead to moderate reductions in midgut alkalization. However, these reductions in midgut pH do not affect the immune response or resilience of sea urchin larvae to a Vibrio infection under ocean acidification conditions. Our study addressed the evolutionary benefits of the alkaline midgut of Ambulacraria larval stages. The data indicate that alkaline conditions in the gut may serve as a first defensive barrier against environmental pathogens and that this mechanism can compensate for changes in seawater pH.

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“…Given the potential role of SpSlc9a2 in supporting nutrient uptake, its upregulation under ocean acidification simulations can be hypothesized to be a consequence of enhanced nutrient absorption rather than acid-base regulation. Finally, infection of pluteus larvae with Vibrio diazotrophicus led to an accumulation of bacteria in the gut (Ho et al, 2016;Buckley and Rast, 2019;Stumpp et al, 2020) accompanied by increased NHE-2 expression (Stumpp et al, 2020). Here it can be also suggested that a large fraction of ingested bacteria is digested and the free nutrients stimulate NHE-2 expression for the H + -coupled nutrient uptake.…”

Section: Effects Of Seawater Acidification On Midgut Ph and Na + Regulationmentioning

confidence: 88%

Na+/H+ exchangers differentially contribute to midgut fluid sodium and proton concentration in the sea urchin larva

Petersen

Chang

2021

Journal of Experimental Biology

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Regulation of ionic composition and pH is a requisite of all digestive systems in the animal kingdom. Larval stages of the marine superphylum ambulacraria, including echinoderms and hemichordates, were demonstrated to have highly alkaline conditions in their midgut with the underlying epithelial transport mechanisms being largely unknown.Using ion-selective microelectrodes, the present study demonstrated that pluteus larvae of the purple sea urchin have highly alkaline pH (pH ∼9) and low [Na+] ( ̴120 mM) in their midgut fluids, compared to the ionic composition of the surrounding sea water. We pharmacologically investigated the role of Na+/H+-exchangers in intracellular pH regulation and midgut proton and sodium maintenance using the NHE inhibitor 5-(n-ethyl-n-isopropyl)amiloride (EIPA). Basolateral EIPA application decreased midgut pH while luminal application, via micro-injections increased midgut [Na+], without affecting pH. Immunohistochemical analysis demonstrated a luminal localization of NHE-2 (SpSlc9a2) in the midgut epithelium. Specific knockdown of spslc9a2 using vivo morpholinos led to an increase in midgut [Na+] without affecting pH. Acute acidification experiments in combination with qPCR analysis and measurements of midgut pH and [Na+] identified two other NHE isoforms, Spslc9a7 and SpSlc9a8 that potentially contribute to the regulation of [Na+] and pH in midgut fluids.This work provides new insights to ion regulatory mechanisms in the midgut epithelium of sea urchin larvae. The involvement of NHEs in regulating pH and Na+ balance in midgut fluids shows conserved features to insect and vertebrate digestive systems and may contribute to the ability of sea urchin larvae to cope with changes in seawater pH.

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Immune activity at the gut epithelium in the larval sea urchin

Cited by 28 publications

References 37 publications

Genetic manipulation of the pigment pathway in a sea urchin reveals distinct lineage commitment prior to metamorphosis in the bilateral to radial body plan transition

Genetic manipulation of the pigment pathway in a sea urchin reveals distinct lineage commitment prior to metamorphosis in the bilateral to radial body plan transition

Alkaline guts contribute to immunity during exposure to acidified seawater in the sea urchin larva

Na+/H+ exchangers differentially contribute to midgut fluid sodium and proton concentration in the sea urchin larva

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