Experimental manipulation of microbiota reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm

Fontaine, Samantha S; Mineo, Patrick M.; Kohl, Kevin D.

doi:10.1038/s41559-022-01686-2

Cited by 39 publications

(56 citation statements)

References 121 publications

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“…For example, Santoro et al (2021) demonstrated that the stability of inoculated “beneficial microorganisms” in the coral Mussismilia hispida provided a thermal protection effect, reducing heat stress and preventing the associated mortality (40% increase in the survival rate) of the hosts. Contrary, disruptions in the microbiome structure and function can lead to a weakened thermal tolerance and performance of the host, and a decrease in survival rate under prolonged heat stress condition, particularly in early ontogenetic stages such as in the tadpoles of the green frog Lithobates clamitans (Fontaine et al, 2022). Overall, regardless of the mechanisms, the temporal stability in the microbiome structure and function found in this study may imply a fundamental ecological role for I. nucleus survival in the thermally extreme tropical intertidal environment (Bang et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Thermal fluctuations independently modulate physiological plasticity and the dynamics of the gut microbiome in a tropical rocky shore oyster

Arromrak

Wong

Hui

et al. 2023

Preprint

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Extreme thermal conditions on rocky shores are challenging to the survival of intertidal ectotherms, especially during emersion periods. Yet, many species are highly successful in these environments in part due to their ability to regulate intrinsic mechanisms associated with physiological stress and their metabolic demands. More recently, there has been a growing awareness that other extrinsic mechanisms, such as animal-associated microbial communities, can also influence the tolerance and survival of ectotherms under stressful conditions. The extent to which intrinsic and extrinsic mechanisms are functionally linked as part of the overall adaptive response of intertidal animals to temperature change and stress is, however, poorly understood. Here, we examined the dynamics and potential interactions of intrinsic and extrinsic mechanisms in the ecology of the tropical high shore rock oyster, Isognomon nucleus. We found that oysters modulate their internal biochemistry (PUFA-oxidised metabolites including 5-F2t-IsoP, 10-F4t-NeuroP, 13-F4t-NeuroP, and 16-F1t-PhytoP) as part of their adaptive regulation to cope with physiological stress during periods of extreme temperatures when emersed. While we detected extrinsic microbiome changes in alpha diversity, the overall taxonomic and functional structure of the microbiome showed temporal stability with no association with the host biochemical profiles. Our finding here suggests that the microbiome taxonomic and functional structure is maintained by a stable host control (not associated to the host biochemistry) and/or that the microbiome (independent of the host) is resilient to the temperature fluctuations and extremes. This microbiome stability is likely to contribute to the oyster, I. nucleus thermal tolerance, in addition to the intrinsic biochemical adjustment, to survive in the thermally challenging intertidal environment.

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Section: Discussionmentioning

confidence: 99%

Thermal fluctuations independently modulate physiological plasticity and the dynamics of the gut microbiome in a tropical rocky shore oyster

Arromrak

Wong

Hui

et al. 2023

Preprint

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“…However, food is not always plentiful in natural habitats; therefore, warming may negatively affect the fitness of individuals and even populations while maintaining high metabolic rates (e.g., Bestion et al, 2015;Hao et al, 2021;Sun et al, 2022). In contrast, although the metabolism of T. amurensis in the semi-closed habitat was inhibited when the ambient temperature increased (Figure 2D), gut microbiota could assist energic regulation via composition change, which was probably beneficial for the proliferation of microbiota, which in turn assisted the thermal responses of the host (e.g., Seebacher et al, 2014;Fontaine et al, 2022). However, to comprehensively understand this complementary effect, further experimental manipulations are required to confirm the detailed regulation (e.g., Fontaine et al, 2022).…”

Section: Warming Climate Benefit On Gut Microbiota In Both Lizard Spe...mentioning

confidence: 99%

“…In contrast, the gut microbiota has been shown to benefit the host thermoregulation, immunity, metabolism, growth, development, and even social behaviors (e.g., Macke et al, 2017 ; Zhang and Wang, 2022 ), all of which can in turn regulate responses to warming temperatures (e.g., Kearney et al, 2010 ; Triggs and Knell, 2012 ; Montoya-Ciriaco et al, 2020 ). For example, the gut microbiota of tadpoles that experienced 3-week high temperatures (28°C) could modify the metabolism and enhance the heat tolerance of tadpoles ( Fontaine et al, 2022 ). Therefore, how gut microbiota affects the physiological responses of the host to climate warming is complex and still largely controversial ( Bestion et al, 2017 ; Bestion and Cote, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

The divergent effects of moderate climate warming on the gut microbiota and energetic state of cold-climate lizards from open and semi-closed microhabitats

Liu

Yang

et al. 2022

Front. Microbiol.

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IntroductionUnderstanding the physiological responses to warming temperatures is critical for evaluating the vulnerabilities of animals to climate warming. The physiological responses are increasingly affected by gut microbiota. However, the interactions between physiological responses and the gut microbiota of sympatric animals from various microhabitats in the face of climate change remain largely unknown.MethodsTo evaluate the effects of warming temperatures on animals from different microhabitats, we compared locomotor performance, metabolic rate, growth, survival, and gut microbiota of two sympatric ectothermic species (Eremias argus and Takydromus amurensis) from open and semi-closed microhabitats under present and moderate warming climate conditions, respectively.Results and discussionWe found that locomotor performance and growth rates of snout-vent length (SVL) were enhanced in both lizard species by warming climate. Interestingly, warming temperatures enhanced resting metabolic rates (RMR) in the open-habitat lizard, E. argus, but depressed them in the semi-closed habitat lizard, T. amurensis. Reversely, the metabolism-related gut microbiota was not affected by warming in E. argus, whereas it was significantly enhanced by warming in T. amurensis, indicating a plausible compensatory effect of the gut microbiota on the metabolic regulation of T. amurensis. Furthermore, warming likely improved immunity in both lizard species by significantly reducing pathogenic bacteria while increasing probiotics. This study found that high-latitude sympatric lizards from both open and semi-closed habitats were beneficial to warming temperatures by physiological modification and regulation of the gut microbiota and highlighted the importance of integrating the physiology and gut microbiota in evaluating the vulnerability of animals to climate warming.

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“…In one extraordinary example, the host plant's heat tolerance is dependent on both a fungal endophyte and a virus that infects the fungus (Márquez et al 2007). The gut microbiota increased heat tolerance of fruit flies (Jaramillo and Castañeda 2021) and tadpoles (Fontaine et al 2022), and the symbionts of corals increased the thermal tolerance of holobionts (Berkelmans andvan Oppen 2006, Pelosi et al 2021). While the mechanisms of these interactions are not well understood, they alter high-temperature tolerance in a manner consistent with resource change: deprivation reducing Tmax in the case of parasites/pathogens (due to reallocation towards combating infection) and supply increasing Tmax in the case of mutualists.…”

Section: The Dependence Of Tpcs On Environmental Factorsmentioning

confidence: 99%

Are we underestimating the ecological and evolutionary effects of warming? Interactions with other environmental drivers may increase species vulnerability to high temperatures

Litchman¹,

Thomas²

2022

Preprint

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Warming, the most prominent aspect of global environmental change, already affects most ecosystems on Earth. In recent years, biologists have increasingly integrated the effects of warming into their models by capturing how temperature shapes their physiology, ecology, behavior, evolutionary adaptation, and probability of extirpation/extinction. The more physiologically-grounded approaches to predicting ectotherms’ responses use thermal performance curves (TPCs) obtained by measuring species performance (e.g., growth rate) under different temperatures while other factors are held constant. These other factors are usually held at benign levels to ‘isolate’ the effects of temperature. Here we highlight that this practice may paint a misleading picture because TPCs are functions of other factors, including global change stressors. We review evidence that resource limitation, pH, oxygen and CO2 concentration, water availability, as well as parasites, all influence TPC shape and thermal traits such as optimum temperature for growth. Evidence from a wide variety of organisms – phytoplankton, protists, plants, insects, and fish – points towards such interactions increasing organisms’ susceptibility to high temperatures. Failing to account for these interactions is likely to lead to erroneous predictions of performance in nature and possibly an underestimation of the risks of warming. We discuss the general patterns and possible consequences of such interactions for ecological communities. But importantly, interactions with TPCs share common features that we can learn from. Incorporating these interactions into population and community models should lead to deeper insights and more accurate predictions of species’ performance in nature, now and in the future.

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Experimental manipulation of microbiota reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm

Cited by 39 publications

References 121 publications

Thermal fluctuations independently modulate physiological plasticity and the dynamics of the gut microbiome in a tropical rocky shore oyster

Thermal fluctuations independently modulate physiological plasticity and the dynamics of the gut microbiome in a tropical rocky shore oyster

The divergent effects of moderate climate warming on the gut microbiota and energetic state of cold-climate lizards from open and semi-closed microhabitats

Are we underestimating the ecological and evolutionary effects of warming? Interactions with other environmental drivers may increase species vulnerability to high temperatures

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