Experimental temperatures shape host microbiome diversity and composition

Li, Jingdi; Bates, Kieran A.; Hoang, Kim Le Mai; Hector, Tobias E.; Knowles, Sarah C. L.; King, Kayla C.

doi:10.1111/gcb.16429

Cited by 31 publications

(23 citation statements)

References 146 publications

(150 reference statements)

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“…Host-associated microbiome diversity, structure, and functions are more frequently considered as important components of animal adaptation and acclimation to environmental change (Bang et al, 2018; Foster et al, 2017; Voolstra and Ziegler, 2020). Alterations in microbiome diversity can be associated with the direct influence of the host’s physiology and/or with host-independent environmental effects (Li et al, 2018; Li et al, 2022; Muñoz et al, 2019; Shiu et al, 2017). In our study, the composition and diversity (ASV richness and Shannon diversity) of the oyster gut-associated microbiome varied with time which coincided with variation in the oyster’s body temperature, suggesting that the thermal condition experienced by the host may modulate the microbial alpha diversity via either direct/indirect physio-biochemical influences (Apprill, 2017; Pita et al, 2018; Sorek et al, 2014).…”

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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“…In nature, the animals that the global climate change will affect at most are ectotherms partly because their performance were significantly affected by daily temperature fluctuations ( Paaijmans et al, 2013 ; Pincebourde and Casas, 2015 ; Rozen-Rechels et al, 2019 ). Therefore, studies on short-term changes in environmental temperature in ectotherm physiology are urgently needed, including microbial communities that play important roles in host health and respond relatively quickly to changes in the environmental conditions ( McFall-Ngai et al, 2013 ; Horlick et al, 2020 ; Li J. et al, 2022 ). In the present study, we examined how temporal temperature variation affects gut microbial community composition in two fish species (the common carp and largemouth bass) by an increase in environmental temperature at three time points (ranging from 24 to 168 h).…”

Section: Discussionmentioning

confidence: 99%

Gut microbiota of two invasive fishes respond differently to temperature

Zhang

Yang

et al. 2023

Front. Microbiol.

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Temperature variation structures the composition and diversity of gut microbiomes in ectothermic animals, key regulators of host physiology, with potential benefit to host or lead to converse results (i.e., negative). So, the significance of either effect may largely depend on the length of time exposed to extreme temperatures and how rapidly the gut microbiota can be altered by change in temperature. However, the temporal effects of temperature on gut microbiota have rarely been clarified. To understand this issue, we exposed two juvenile fishes (Cyprinus carpio and Micropterus salmoides), which both ranked among the 100 worst invasive alien species in the world, to increased environmental temperature and sampled of the gut microbiota at multiple time points after exposure so as to determine when differences in these communities become detectable. Further, how temperature affects the composition and function of microbiota was examined by comparing predicted metagenomic profiles of gut microbiota between treatment groups at the final time point of the experiment. The gut microbiota of C. carpio was more plastic than those of M. salmoides. Specifically, communities of C. carpio were greatly altered by increased temperature within 1 week, while communities of M. salmoides exhibit no significant changes. Further, we identified 10 predicted bacterial functional pathways in C. carpio that were temperature-dependent, while none functional pathways in M. salmoides was found to be temperature-dependent. Thus, the gut microbiota of C. carpio was more sensitive to temperature changes and their functional pathways were significantly changed after temperature treatment. These results showed the gut microbiota of the two invasive fishes differ in response to temperature change, which may indicate that they differ in colonization modes. Broadly, we have confirmed that the increased short-term fluctuations in temperatures are always expected to alter the gut microbiota of ectothermic vertebrates when facing global climate change.

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“…In invertebrates, warming typically results in increases in Proteobacteria and decreases in Actinobacteria (Sepulveda & Moeller, 2020). Further, a recent meta‐analysis revealed that warmer mean temperatures impact microbial communities by affecting their phylogenetic diversity and community composition but not dispersion (Li et al, 2023). Beyond illustrating that environmental change can lead to disturbance in microbial communities, it is important to determine the underlying mechanisms by which these changes ultimately impact host fitness (Brüssow, 2020).…”

Section: Mean Environmental Temperaturementioning

confidence: 99%

“…Many studies which have assessed the effects of mean temperature increases on animal gut microbiota do so through short‐term exposure, which can be considered analogous to exposing animals to heat waves (Sepulveda & Moeller, 2020). Therefore, findings from studies of mean temperature change are often informative for understanding the effects of heat waves, especially those that use realistic temperature regimes (e.g., ramping temperatures as opposed to static temperature shifts; Li et al, 2023). A meta‐analysis of studies testing increases in mean temperature with ramping regimes showed that longer exposure time does not exacerbate reduction in microbial community diversity but can lead to more substantial community composition divergence compared to control groups (Li et al, 2023).…”

Section: Temperature Variabilitymentioning

confidence: 99%

Climate change is not just global warming: Multidimensional impacts on animal gut microbiota

Williams

Logan

2023

Microbial Biotechnology

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Climate change has rapidly altered many ecosystems, with detrimental effects for biodiversity across the globe. In recent years, it has become increasingly apparent that the microorganisms that live in and on animals can substantially affect host health and physiology, and the structure and function of these microbial communities can be highly sensitive to environmental variables. To date, most studies have focused on the effects of increasing mean temperature on gut microbiota, yet other aspects of climate are also shifting, including temperature variation, seasonal dynamics, precipitation and the frequency of severe weather events. This array of environmental pressures might interact in complex and non‐intuitive ways to impact gut microbiota and consequently alter animal fitness. Therefore, understanding the impacts of climate change on animals requires a consideration of multiple types of environmental stressors and their interactive effects on gut microbiota. Here, we present an overview of some of the major findings in research on climatic effects on microbial communities in the animal gut. Although ample evidence has now accumulated that shifts in mean temperature can have important effects on gut microbiota and their hosts, much less work has been conducted on the effects of other climatic variables and their interactions. We provide recommendations for additional research needed to mechanistically link climate change with shifts in animal gut microbiota and host fitness.

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Experimental temperatures shape host microbiome diversity and composition

Cited by 31 publications

References 146 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

Gut microbiota of two invasive fishes respond differently to temperature

Climate change is not just global warming: Multidimensional impacts on animal gut microbiota

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