Beat the heat: correlates, compounds, and mechanisms involved in fungal thermotolerance

Mattoon, Ellie Rose; Casadevall, Arturo; Cordero, Radamés J. B.

doi:10.1016/j.fbr.2021.03.002

Cited by 21 publications

(17 citation statements)

References 144 publications

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“…The genetic mechanisms underlying thermal tolerance have been examined in several fungal species. Though some genes and mutations can have major effects on thermal tolerance ( 41 ), most studies have shown that thermotolerance is a polyphyletic trait that emerged multiple times throughout the fungal phylogeny ( 30 , 42 ). Our BSH results suggested genetic differences between strains contributed to variations in thermal growth profiles among strains of A. fumigatus .…”

Section: Discussionmentioning

confidence: 99%

Assessing thermal adaptation of a global sample of Aspergillus fumigatus: Implications for climate change effects

Korfanty

Heifetz

2023

Front. Public Health

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Aspergillus fumigatus is a common environmental mold and a major cause of opportunistic infections in humans. It's distributed among many ecological niches across the globe. A major virulence factor of A. fumigatus is its ability to grow at high temperature. However, at present, little is known about variations among strains in their growth at different temperatures and how their geographic origins may impact such variations. In this study, we analyzed 89 strains from 12 countries (Cameroon, Canada, China, Costa Rica, France, India, Iceland, Ireland, New Zealand, Peru, Saudi Arabia, and USA) representing diverse geographic locations and temperature environments. Each strain was grown at four temperatures and genotyped at nine microsatellite loci. Our analyses revealed a range of growth profiles, with significant variations among strains within individual geographic populations in their growths across the temperatures. No statistically significant association was observed between strain genotypes and their thermal growth profiles. Similarly geographic separation contributed little to differences in thermal adaptations among strains and populations. The combined analyses among genotypes and growth rates at different temperatures in the global sample suggest that most natural populations of A. fumigatus are capable of rapid adaptation to temperature changes. We discuss the implications of our results to the evolution and epidemiology of A. fumigatus under increasing climate change.

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Section: Discussionmentioning

confidence: 99%

Assessing thermal adaptation of a global sample of Aspergillus fumigatus: Implications for climate change effects

Korfanty

Heifetz

2023

Front. Public Health

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“…As reported, there exist multiple evolutionary trajectories for fungi to acquire the fitness of growth under high temperature (Mattoon et al , 2021). With integrative analysis of large‐scale genomics and trait data in yeast, we could infer amounts of potential gene features relevant for the formation of thermotolerance at a systems level.…”

Section: Discussionmentioning

confidence: 99%

Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection

Yuan

et al. 2021

Molecular Systems Biology

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Yeasts are known to have versatile metabolic traits, while how these metabolic traits have evolved has not been elucidated systematically. We performed integrative evolution analysis to investigate how genomic evolution determines trait generation by reconstructing genome-scale metabolic models (GEMs) for 332 yeasts. These GEMs could comprehensively characterize trait diversity and predict enzyme functionality, thereby signifying that sequence-level evolution has shaped reaction networks towards new metabolic functions. Strikingly, using GEMs, we can mechanistically map different evolutionary events, e.g. horizontal gene transfer and gene duplication, onto relevant subpathways to explain metabolic plasticity. This demonstrates that gene family expansion and enzyme promiscuity are prominent mechanisms for metabolic trait gains, while GEM simulations reveal that additional factors, such as gene loss from distant pathways, contribute to trait losses. Furthermore, our analysis could pinpoint to specific genes and pathways that have been under positive selection and relevant for the formulation of complex metabolic traits, i.e. thermotolerance and the Crabtree effect. Our findings illustrate how multidimensional evolution in both metabolic network structure and individual enzymes drives phenotypic variations.

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“…The abundant trehalose production contributed to the cross-protection of salt stress for the thermotolerance of P. kudriavzevii . Glycerol overproduction helps yeast cells cope with the adverse effects of heat stress, such as protecting proteins from thermal denaturation [ 26 ]. Faster glycerol production was found in thermotolerant yeast strains than thermosensitive strains [ 27 ].…”

Section: Discussionmentioning

confidence: 99%

“…Heat stress can induce the ROS outburst in cells, causing pleiotropic damage of biomolecules which may result in cell death [ 26 ]. In this study, obvious heat-induced ROS generation was also found in P. kudriavzevii (Fig.…”

Section: Discussionmentioning

confidence: 99%

Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage

Liu

Wang

et al. 2021

Biotechnol Biofuels

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Background High-temperature bioethanol production benefits from yeast thermotolerance. Salt stress could induce obvious cross-protection against heat stress of Pichia kudriavzevii, contributing to the improvement of its thermotolerance and bioethanol fermentation. However, the underlying mechanisms of the cross-protection remain poorly understood. Results Salt stress showed obvious cross-protection for thermotolerance and high-temperature ethanol production of P. kudriavzevii observed by biomass, cell morphology and bioethanol production capacity. The biomass and ethanol production of P. kudriavzevii at 45 °C were, respectively, improved by 2.6 and 3.9 times by 300 mmol/L NaCl. Metabolic network map showed that salt stress obviously improved the key enzymes and intermediates in carbohydrate metabolism, contributing to the synthesis of bioethanol, ATP, amino acids, nucleotides, and unsaturated fatty acids, as well as subsequent intracellular metabolisms. The increasing trehalose, glycerol, HSPs, and ergosterol helped maintain the normal function of cell components. Heat stress induced serious oxidative stress that the ROS-positive cell rate and dead cell rate, respectively, rose from 0.5% and 2.4% to 28.2% and 69.2%, with the incubation temperature increasing from 30 to 45 °C. The heat-induced ROS outburst, oxidative damage, and cell death were obviously inhibited by salt stress, especially the dead cell rate which fell to only 20.3% at 300 mmol/L NaCl. The inhibiting oxidative damage mainly resulted from the abundant synthesis of GSH and GST, which, respectively, increased by 4.8 and 76.1 times after addition of 300 mmol/L NaCl. The improved bioethanol production was not only due to the improved thermotolerance, but resulted from the up-regulated alcohol dehydrogenases and down-regulated aldehyde dehydrogenases by salt stress. Conclusion The results provide a first insight into the mechanisms of the improved thermotolerance and high-temperature bioethanol production of P. kudriavzevii by salt stress, and provide important information to construct genetic engineering yeasts for high-temperature bioethanol production. Graphical Abstract

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Beat the heat: correlates, compounds, and mechanisms involved in fungal thermotolerance

Cited by 21 publications

References 144 publications

Assessing thermal adaptation of a global sample of Aspergillus fumigatus: Implications for climate change effects

Assessing thermal adaptation of a global sample of Aspergillus fumigatus: Implications for climate change effects

Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection

Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage

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