Unraveling the predictive role of temperature in the gut microbiota of the sea urchin <i>Echinometra</i> sp. <i>EZ</i> across spatial and temporal gradients

Ketchum, Remi N.; Smith, Edward G.; Vaughan, Grace O.; McParland, Dain; Al-Mansoori, Noura; Burt, John A.; Reitzel, Adam M.

doi:10.1111/mec.15990

Cited by 8 publications

(7 citation statements)

References 74 publications

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“…Although these results contrast with previous experimental studies on adult urchins (spines, gut) showing that the urchin microbial community is stable under exposure to OW/OA (Brothers et al, 2018; Webster et al, 2016), the discrepancy in microbial responses may be explained by the different tissue types as well as the extended exposure periods investigated within this study. Indeed, Ketchum et al (2021) recently confirmed that temperature‐driven microbial shifts occur in the gut of the urchin Echinometra sp. EZ in natural conditions, suggesting that temperature can be a predictor of community variation.…”

Section: Discussionmentioning

confidence: 96%

“…Sea urchins are an emerging model for investigating animal–microbe symbiosis (Carrier et al, 2021), showing a re‐shaping of the bacterial communities during major developmental transitions, from pelagic larvae to benthic juveniles and adults, with microbes inferred to contribute to larval immunity and nutrition in some species (Carrier et al, 2021; Carrier & Reitzel, 2019, 2020; Schuh et al, 2020). Urchins are susceptible to changing climate, in particular, during larval life stages (Byrne & Przeslawski, 2013), though little is known about the effects of OW and OA on microbial dynamics in adult urchins and early developmental stages (Brothers et al, 2018; Carrier & Reitzel, 2020; Ketchum et al, 2021; Webster et al, 2016). Along with an important role in reef resilience through its grazing activity, Echinometra sp.…”

Section: Introductionmentioning

confidence: 99%

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Life‐stage specificity and cross‐generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Marangon,

Uthicke,

Patel

et al. 2023

Molecular Ecology

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Microbes play a critical role in the development and health of marine invertebrates, though microbial dynamics across life stages and host generations remain poorly understood in most reef species, especially in the context of climate change. Here, we use a 4‐year multigenerational experiment to explore microbe–host interactions under the Intergovernmental Panel on Climate Change (IPCC)‐forecast climate scenarios in the rock‐boring tropical urchin Echinometra sp. A. Adult urchins (F0) were exposed for 18 months to increased temperature and pCO2 levels predicted for years 2050 and 2100 under RCP 8.5, a period which encompassed spawning. After rearing F1 offspring for a further 2 years, spawning was induced, and F2 larvae were raised under current day and 2100 conditions. Cross‐generational climate effects were also explored in the microbiome of F1 offspring through a transplant experiment. Using 16S rRNA gene sequence analysis, we determined that each life stage and generation was associated with a distinct microbiome, with higher microbial diversity observed in juveniles compared to larval stages. Although life‐stage specificity was conserved under climate conditions projected for 2050 and 2100, we observed changes in the urchin microbial community structure within life stages. Furthermore, we detected a climate‐mediated parental effect when juveniles were transplanted among climate treatments, with the parental climate treatment influencing the offspring microbiome. Our findings reveal a potential for cross‐generational impacts of climate change on the microbiome of a tropical invertebrate species.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Life‐stage specificity and cross‐generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Marangon,

Uthicke,

Patel

et al. 2023

Molecular Ecology

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“…Microbiome assembly depends on the host's evolutionary history and the environment [38][39][40][41]. One of these two factors is often more influential [39,40], but which host gene(s) or environmental parameter(s) influences these interactions often remains elusive (but see [42,43]). Furthermore, recent efforts have increased the availability of hologenomes to enable the underlying genetic factors of these evolutionarily ancient partnerships to be determined [41,[44][45][46].…”

Section: Discussionmentioning

confidence: 99%

Pigmentation biosynthesis influences the microbiome in sea urchins

et al. 2022

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Organisms living on the seafloor are subject to encrustations by a wide variety of animals, plants and microbes. Sea urchins, however, thwart this covering. Despite having a sophisticated immune system, there is no clear molecular mechanism that allows sea urchins to remain free of epibiotic microorganisms. Here, we test the hypothesis that pigmentation biosynthesis in sea urchin spines influences their interactions with microbes in vivo using CRISPR/Cas9. We report three primary findings. First, the microbiome of sea urchin spines is species-specific and much of this community is lost in captivity. Second, different colour morphs associate with bacterial communities that are similar in taxonomic composition, diversity and evenness. Lastly, loss of the pigmentation biosynthesis genes polyketide synthase and flavin-dependent monooxygenase induces a shift in which bacterial taxa colonize sea urchin spines. Therefore, our results are consistent with the hypothesis that host pigmentation biosynthesis can, but may not always, influence the microbiome in sea urchin spines.

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“…Similar results reported in the sea urchin ( Echinometra sp. EZ ) with gut microbiota varying across thermally variable habitats and displaying temporal shifts correlated with temperature ( Ketchum et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Effect of long-term temperature stress on the intestinal microbiome of an invasive snail

Qian

Gao

et al. 2022

Front. Microbiol.

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The gut microbiome is vital to the physiological and biochemical functions of the host, and changes in the composition of these microbial communities may affect growth and adaptability to the environment. Pomacea canaliculata is an invasive freshwater snail which has become a serious agricultural pest. Temperature adaptation is considered an important reason for the widespread distribution of this species. To date, the contribution of the gut microbes to host fitness of P. canaliculata during long-term temperature stress is not well understood. In this study, the morphological changes and intestinal microbiome of P. canaliculata under long-term stress at low temperature (15°C) and high temperature (35°C) were investigated with laboratory experiments. Compared with control group (25°C), the alpha diversity increased and pathogenic bacteria enriched changed under high and low temperature stress. The effect of high temperature stress on the intestinal microbiome of P. canaliculata was more significant than that of low temperature stress. A sustained high temperature environment led to an increase in the abundance of pathogenic bacteria, such as Aeromonas and Enterobacter, and a decrease in the abundance of immune-related bacteria such as Bacteroidetes, Firmicutes, and Lactococcus. These intestine microbiome changes can increase the risk of diseases like intestinal inflammation, and lead to more deaths at high temperature environments. In addition, with the extension of stress time from 14 to 28 days, the beneficial bacteria such as Bacteroidetes, Firmicutes, and Lactococcus were significantly enriched, while potential pathogenic bacteria such as Pseudomonas, Acinetobacter, Shivalella, and Flavobacterium decreased, suggesting that intestinal microbiota may play an important role in host response to heat stress. These results are consistent with previously reported results that the survival rate of both male and female P. canaliculata no longer significantly reduced after 21 days of high temperature stress, suggesting that the surviving P. canaliculata had gradually adapted to high temperature environments under long-term high temperature stress.

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Unraveling the predictive role of temperature in the gut microbiota of the sea urchin Echinometra sp. EZ across spatial and temporal gradients

Abstract: The microbiome is important in shaping organismal biology in a wide range of eukaryotic species and has been shown to play critical roles in host physiological functions and susceptibility to disease (Bayer

Cited by 8 publications

References 74 publications

Life‐stage specificity and cross‐generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Life‐stage specificity and cross‐generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Pigmentation biosynthesis influences the microbiome in sea urchins

Effect of long-term temperature stress on the intestinal microbiome of an invasive snail

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