Gene fusion and functional diversification of P450 genes facilitate thermophilic fungal adaptation to temperature change
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ABSTRACT:
SUBMITTER: Li S
PROVIDER: S-EPMC11376295 | biostudies-literature | 2024 Apr
REPOSITORIES: biostudies-literature
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Project description:The ecological importance of the duplication and diversification of gene clusters that synthesize secondary metabolites in fungi remains poorly understood. Here, we demonstrated that the duplication and subsequent diversification of a gene cluster produced two polyketide synthase gene clusters in the cosmopolitan fungal genus Metarhizium. Diversification occurred in the promoter regions and the exon-intron structures of the two Pks paralogs (Pks1 and Pks2). These two Pks genes have distinct expression patterns, with Pks1 highly expressed during conidiation and Pks2 highly expressed during infection. Different upstream signaling pathways were found to regulate the two Pks genes. Pks1 is positively regulated by Hog1-MAPK, Slt2-MAPK and Mr-OPY2, while Pks2 is positively regulated by Fus3-MAPK and negatively regulated by Mr-OPY2. Pks1 and Pks2 have been subjected to positive selection and synthesize different secondary metabolites. PKS1 is involved in synthesis of an anthraquinone derivative, and contributes to conidial pigmentation, which plays an important role in fungal tolerance to UV radiation and extreme temperatures. Disruption of the Pks2 gene delayed formation of infectious structures and increased the time taken to kill insects, indicating that Pks2 contributes to pathogenesis. Thus, the duplication of a Pks gene cluster and its subsequent functional diversification has increased the adaptive flexibility of Metarhizium species.
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Project description:Citrus target spot, caused by Pseudofabraea citricarpa, was formerly considered a cold-tolerant fungal disease. However, it has now spread from high-latitude regions to warmer low-latitude regions. Here, we conducted physiological observations on two different strains of the fungus collected from distinct regions, and evaluated their pathogenicity. Interestingly, the CQWZ collected from a low-latitude orchard, exhibited higher temperature tolerance and pathogenicity when compared to the SXCG collected from a high-latitude orchard. To further understand the evolution of temperature tolerance and virulence in these pathogens during the spread process, as well as the mechanisms underlying these differences, we performed genomic comparative analysis. The genome size of CQWZ was determined to be 44,004,669 bp, while the genome size of SXCG was determined to be 45,377,339 bp. Through genomic collinearity analysis, we identified two breakpoints and rearrangements during the evolutionary process of these two strains. Moreover, gene annotation results revealed that the CQWZ possessed 376 annotated genes in the "Xenobiotics biodegradation and metabolism" pathway, which is 79 genes more than the SXCG. The main factor contributing to this difference was the presence of salicylate hydroxylase. We also observed variations in the oxidative stress pathways and core pathogenic genes. The CQWZ exhibited the presence of a heat shock protein (HSP SSB), a catalase (CAT2), and 13 core pathogenic genes, including a LysM effector, in comparison to the SXCG. Furthermore, there were significant disparities in the gene clusters responsible for the production of seven metabolites, such as Fumonisin and Brefeldin. Finally, we identified the regulatory relationship, with the HOG pathway at its core, that potentially contributes to the differences in thermotolerance and virulence. As the global climate continues to warm, crop pathogens are increasingly expanding to new territories. Our findings will enhance understanding of the evolution mechanisms of pathogens under climate change.
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Project description:Thermophilic xylanases from hot-spring microorganisms play potential biological and industrial applications for renewable and sustainable social development. However, high-temperature adaptation mechanisms of these thermophilic xylanases remain elusive at the molecular and evolutionary levels. Here, two recently reported xylanases, named XynDRTY1 and XynM1, from hot springs were subjected to molecular dynamics (MD) simulations at a series of temperature gradients and comparatively analyzed in comparison with the evolutionary background of the xylanase family. Comparative analysis of MD trajectories revealed that the XynM1 exhibits smaller structural dynamics and greater thermal stability than the XynDRTY1, although both share a similar fold architecture with structural differences in the βα_loops. Local regions whose conformational flexibility and regular secondary structure exhibited differences as temperature increases were closely related to the high-temperature adaptation of xylanase, implying that stabilization of these regions is a feasible strategy to improve the thermal stability of xylanases. Furthermore, coevolutionary information from the xylanase family further specified the structural basis of xylanases. Thanks to these results about the sequence, structure, and dynamics of thermophilic xylanases from hot springs, a series of high-temperature-related structural determinants were resolved to promote understanding of the molecular mechanism of xylanase high-temperature adaptation and to provide direct assistance in the improvement of xylanase thermal stability.
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Project description:Chitinases enzymatically hydrolyze chitin, a highly abundant and utilized polymer of N-acetyl-glucosamine. Fungi are a rich source of chitinases; however, the phylogenetic and functional diversity of fungal chitinases are not well understood. We surveyed fungal chitinases from 373 publicly available genomes, characterized domain architecture, and conducted phylogenetic analyses of the glycoside hydrolase (GH18) domain. This large-scale analysis does not support the previous division of fungal chitinases into three major clades (A, B, C) as chitinases previously assigned to the "C" clade are not resolved as distinct from the "A" clade. Fungal chitinase diversity was partly shaped by horizontal gene transfer, and at least one clade of bacterial origin occurs among chitinases previously assigned to the "B" clade. Furthermore, chitin-binding domains (including the LysM domain) do not define specific clades, but instead are found more broadly across clades of chitinases. To gain insight into biological function diversity, we characterized all eight chitinases (Cts) from the thermally dimorphic fungus, Histoplasma capsulatum: six A clade, one B clade, and one formerly classified C clade chitinases. Expression analyses showed variable induction of chitinase genes in the presence of chitin but preferential expression of CTS3 in the mycelial stage. Activity assays demonstrated that Cts1 (B-I), Cts2 (A-V), Cts3 (A-V), Cts4 (A-V) have endochitinase activities with varying degrees of chitobiosidase function. Cts6 (C-I) has activity consistent with N-acetyl-glucosaminidase exochitinase function and Cts8 (A-II) has chitobiase activity. These results suggest chitinase activity is variable even within subclades and that predictions of functionality require more sophisticated models.
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Project description:BackgroundGlobal climate change significantly impacts ecosystems, particularly through temperature fluctuations that affect insect physiology and behavior. As poikilotherms, insect pests such as the globally devastating diamondback moth (DBM), Plutella xylostella, are especially vulnerable to rising temperatures and extreme heat events, necessitating effective adaptive mechanisms.ResultsHere we demonstrate the roles of zinc finger proteins (ZFPs) in mediating thermal adaptability in DBM. We utilized a comprehensive approach involving cloning and bioinformatics analysis of three ZFPs, PxZNF568, PxZNF93, and PxZNF266, measurement of their expression levels in hot-evolved and control strains, and assessment of catalase enzymatic activity and total antioxidant capacity. We also employed CRISPR/Cas9 technology to create five stable homozygous knockout strains to elucidate ZFP functions in high-temperature tolerance. Survival rates under high-temperature stress and the critical thermal maxima (CTMax) of the knockout strains were significantly lower than the wild-type strain, and exhibited marked decreases in antioxidant capacity.ConclusionFindings reveal the importance of ZFPs in thermal adaptability of DBM, contributing critical insights for future pest management strategies in the context of a warming climate and laying the foundation for further exploration of ZFP functionality in agricultural pest control.
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Project description:BackgroundGene duplication is the primary source of new genes with novel or altered functions. It is known that duplicates may obtain these new functional roles by evolving divergent expression patterns and/or protein functions after the duplication event. Here, using yeast (Saccharomyces cerevisiae) as a model organism, we investigate a previously little considered mode for the functional diversification of duplicate genes: subcellular adaptation of encoded proteins.ResultsWe show that for 24-37% of duplicate gene pairs derived from the S. cerevisiae whole-genome duplication event, the two members of the pair encode proteins that localize to distinct subcellular compartments. The propensity of yeast duplicate genes to evolve new localization patterns depends to a large extent on the biological function of their progenitor genes. Proteins involved in processes with a wider subcellular distribution (for example, catabolism) frequently evolved new protein localization patterns after duplication, whereas duplicate proteins limited to a smaller number of organelles (for example, highly expressed biosynthesis/housekeeping proteins with a slow rate of evolution) rarely relocate within the cell. Paralogous proteins evolved divergent localization patterns by partitioning of ancestral localizations ('sublocalization'), but probably more frequently by relocalization to new compartments ('neolocalization'). We show that such subcellular reprogramming may occur through selectively driven substitutions in protein targeting sequences. Notably, our data also reveal that relocated proteins functionally adapted to their new subcellular environments and evolved new functional roles through changes of their physico-chemical properties, expression levels, and interaction partners.ConclusionWe conclude that protein subcellular adaptation represents a common mechanism for the functional diversification of duplicate genes.
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Project description:BACKGROUND:Cytochrome P450 enzymes play critical roles in fungal biology and ecology. To support studies on the roles and evolution of cytochrome P450 enzymes in fungi based on rapidly accumulating genome sequences from diverse fungal species, an efficient bioinformatics platform specialized for this super family of proteins is highly desirable. RESULTS:The Fungal Cytochrome P450 Database (FCPD) archives genes encoding P450s in the genomes of 66 fungal and 4 oomycete species (4,538 in total) and supports analyses of their sequences, chromosomal distribution pattern, and evolutionary histories and relationships. The archived P450s were classified into 16 classes based on InterPro terms and clustered into 141 groups using tribe-MCL. The proportion of P450s in the total proteome and class distribution in individual species exhibited certain taxon-specific characteristics. CONCLUSION:The FCPD will facilitate systematic identification and multifaceted analyses of P450s at multiple taxon levels via the web. All data and functions are available at the web site http://p450.riceblast.snu.ac.kr/.
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Project description:IntroductionExtreme heat is a significant cause of morbidity and mortality, and the incidence of acute heat illness (AHI) will likely increase secondary to anthropogenic climate change. Prompt diagnosis and treatment of AHI are critical; however, relevant diagnostic and surveillance tools have received little attention. In this exploratory cross-sectional and diagnostic accuracy study, we evaluated three tools for use in the prehospital setting: 1) case definitions; 2) portable loggers to measure on-scene heat exposure; and 3) prevalence data for potential AHI risk factors.MethodsWe enrolled 480 patients who presented to emergency medical services with chief complaints consistent with AHI in Ahmedabad, India, from April-June 2016 in a cross-sectional study. We evaluated AHI case definition test characteristics in reference to trained prehospital provider impressions, compared on-scene heat index measured by portable loggers to weather station measurements, and identified AHI behavioral and environmental risk factors using logistic regression.ResultsThe case definition for heat exhaustion was 23.8% (12.1-39.5%) sensitive and 93.6% (90.9-95.7%) specific. The positive and negative predictive values were 33.5% (20.8-49.0%) and 90.1% (88.5-91.5%), respectively. Mean scene heat index was 6.7°C higher than the mean station heat index (P < 0.001), and station data systematically underestimated heat exposure, particularly for AHI cases. Heat exhaustion cases were associated with on-scene heat index ≥ 49°C (odds ratio [OR] 2.66 [1.13-6.25], P = 0.025) and a history of recent exertion (OR 3.66 [1.30-10.29], P = 0.014), while on-scene air conditioning was protective (OR 0.29 [0.10-0.85], P = 0.024).ConclusionSystematic collection of prehospital data including recent activity history and presence of air conditioning can facilitate early AHI detection, timely intervention, and surveillance. Scene temperature data can be reliably collected and improve heat exposure and AHI risk assessment. Such data may be important elements of surveillance, clinical practice, and climate change adaptation.
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