The Duality of the MAPK Signaling Pathway in the Control of Metabolic Processes and Cellulase Production in Trichoderma reesei

Paula, Renato Graciano de; Antoniêto, Amanda Cristina Campos; Carraro, Cláudia Batista; Lopes, Douglas Christian Borges; Persinoti, Gabriela Félix; Peres, Nalu Teixeira Aguiar; Martinez-Rossi, Nilce Maria; Silva‐Rocha, Rafael; Silva, Roberto Nascimento

doi:10.1038/s41598-018-33383-1

Cited by 34 publications

(25 citation statements)

References 97 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Mitogen-activated protein kinase pathways are conserved signalling cascades in eukaryotes that are involved in the transduction of extracellular or environmental stimuli for transcriptional regulation [ 51 , 52 ]. In fungi, MAPK signalling pathways have been implicated to be involved in a wide range of processes such as fungal pathogenicity, mating, morphogenesis, stress resistance and cell wall integrity [ 53 – 55 ].…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic and proteomic profiling revealed reprogramming of carbon metabolism in acetate-grown human pathogen Candida glabrata

et al. 2021

View full text Add to dashboard Cite

Background Emergence of Candida glabrata, which causes potential life-threatening invasive candidiasis, has been widely associated with high morbidity and mortality. In order to cause disease in vivo, a robust and highly efficient metabolic adaptation is crucial for the survival of this fungal pathogen in human host. In fact, reprogramming of the carbon metabolism is believed to be indispensable for phagocytosed C. glabrata within glucose deprivation condition during infection. Methods In this study, the metabolic responses of C. glabrata under acetate growth condition was explored using high-throughput transcriptomic and proteomic approaches. Results Collectively, a total of 1482 transcripts (26.96%) and 242 proteins (24.69%) were significantly up- or down-regulated. Both transcriptome and proteome data revealed that the regulation of alternative carbon metabolism in C. glabrata resembled other fungal pathogens such as Candida albicans and Cryptococcus neoformans, with up-regulation of many proteins and transcripts from the glyoxylate cycle and gluconeogenesis, namely isocitrate lyase (ICL1), malate synthase (MLS1), phosphoenolpyruvate carboxykinase (PCK1) and fructose 1,6-biphosphatase (FBP1). In the absence of glucose, C. glabrata shifted its metabolism from glucose catabolism to anabolism of glucose intermediates from the available carbon source. This observation essentially suggests that the glyoxylate cycle and gluconeogenesis are potentially critical for the survival of phagocytosed C. glabrata within the glucose-deficient macrophages. Conclusion Here, we presented the first global metabolic responses of C. glabrata to alternative carbon source using transcriptomic and proteomic approaches. These findings implicated that reprogramming of the alternative carbon metabolism during glucose deprivation could enhance the survival and persistence of C. glabrata within the host.

show abstract

Section: Discussionmentioning

confidence: 99%

Transcriptomic and proteomic profiling revealed reprogramming of carbon metabolism in acetate-grown human pathogen Candida glabrata

et al. 2021

View full text Add to dashboard Cite

show abstract

“…Results from transcriptome sequencing (RNA-seq) analysis of T. reesei strains lacking the tmk2 MAPK grown on sugarcane baggase revealed that genes involved in G-protein-related processes are differentially regulated in this background. Among these are the T. reesei GNA-1 homolog as well as three Pth11-like GPCRs and an RGS gene ( 50 ), directly tying G-protein signaling to this MAPK pathway.…”

Section: Discussionmentioning

confidence: 99%

Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in Neurospora crassa

Collier

Ghosh

Borkovich

2020

mBio

View full text Add to dashboard Cite

The filamentous fungus Neurospora crassa decomposes lignocellulosic biomass to generate soluble sugars as carbon sources. In this study, we investigated a role for heterotrimeric G-protein signaling in cellulose degradation. Loss of the Gα subunit genes gna-1 and gna-3, the Gβ subunit genes gnb-1 and cpc-2, the Gγ gene gng-1, or the gene for downstream effector adenylyl cyclase (cr-1) resulted in loss of detectable cellulase activity. This defect was also observed in strains expressing a constitutively active version of gna-3 (gna-3Q208L). We found that GNA-1 levels are greatly reduced in Δgna-3, Δgnb-1, and Δgng-1 strains, likely contributing to cellulase defects in these genetic backgrounds. The observation that gna-3Q208L Δgnb-1 strains exhibit cellulase activity, despite greatly reduced levels of GNA-1 protein, is consistent with positive control of cellulase production by GNA-3 that is manifested in the absence of gnb-1. Expression patterns for five cellulase genes showed that Δgna-1, Δgnb-1, and Δgna-3 mutants produce less cellulase mRNA than the wild type, consistent with transcriptional regulation. Δcpc-2 mutants had wild-type levels of cellulase transcripts, suggesting posttranscriptional control. In contrast, results for Δcr-1 mutants support both transcriptional and posttranscriptional control of cellulase activity by cAMP signaling. Cellulase activity defects in Δgna-3 mutants were fully remediated by cAMP supplementation, consistent with GNA-3 operating upstream of cAMP signaling. In contrast, cAMP addition only partially corrected cellulase activity defects in Δgna-1 and Δgnb-1 mutants, suggesting participation of GNA-1 and GNB-1 in additional cAMP-independent pathways that control cellulase activity. IMPORTANCE Filamentous fungi are critical for the recycling of plant litter in the biosphere by degrading lignocellulosic biomass into simpler compounds for metabolism. Both saprophytic and pathogenic fungi utilize plant cell wall-degrading enzymes to liberate carbon for metabolism. Several studies have demonstrated a role for cellulase enzymes during infection of economically relevant crops by fungal pathogens. Especially in developing countries, severe plant disease means loss of entire crops, sometimes leading to starvation. In this study, we demonstrate that G-protein signaling is a key component of cellulase production. Therefore, understanding the role of G-protein signaling in the regulation of the unique metabolism of cellulose by these organisms can inform innovations in strain engineering of industrially relevant species for biofuel production and in combatting food shortages caused by plant pathogens.

show abstract

“…The strain was maintained at 4 °C on MEX medium [malt extract 3% (w/v) and agar–agar 2% (w/v)], which was supplemented with 5 mM uridine in the case of the pyr4 deletion strain. For all experiments, a spore suspension of QM6aΔ tmus53 Δ pyr4 strain containing 10 6 cells/mL was precultured into 200 mL of Mandels–Andreotti medium [31] supplemented with glycerol 1% (w/v) for 24 h and then transferred to a 200 mL of fresh Mandels–Andreotti medium containing 1% of Avicel [32, 33]. The cultures were incubated on an orbital shaker (200 rpm) at 30 °C for 24, 48, 72, 96 or 120 h. For glucose experiments, the fungus was grown in 2% glucose for 24 h. The resulting culture supernatant was collected by filtration and used for EVs isolation.…”

Section: Methodsmentioning

confidence: 99%

Extracellular vesicles carry cellulases in the industrial fungus Trichoderma reesei

Paula

Antoniêto

Nogueira

et al. 2019

Biotechnol Biofuels

Self Cite

View full text Add to dashboard Cite

Background Trichoderma reesei is the most important industrial producer of lignocellulolytic enzymes. These enzymes play an important role in biomass degradation leading to novel applications of this fungus in the biotechnology industry, specifically biofuel production. The secretory pathway of fungi is responsible for transporting proteins addressed to different cellular locations involving some cellular endomembrane systems. Although protein secretion is an extremely efficient process in T. reesei , the mechanisms underlying protein secretion have remained largely uncharacterized in this organism. Results Here, we report for the first time the isolation and characterization of T. reesei extracellular vesicles (EVs). Using proteomic analysis under cellulose culture condition, we have confidently identified 188 vesicular proteins belonging to different functional categories. Also, we characterized EVs production using transmission electron microscopy in combination with light scattering analysis. Biochemical assays revealed that T. reesei extracellular vesicles have an enrichment of filter paper (FPase) and β-glucosidase activities in purified vesicles from 24, 72 and 96, and 72 and 96 h, respectively. Furthermore, our results showed that there is a slight enrichment of small RNAs inside the vesicles after 96 h and 120 h, and presence of hsp proteins inside the vesicles purified from T. reesei grown in the presence of cellulose. Conclusions This work points to important insights into a better understanding of the cellular mechanisms underlying the regulation of cellulolytic enzyme secretion in this fungus. Electronic supplementary material The online version of this article (10.1186/s13068-019-1487-7) contains supplementary material, which is available to authorized users.

show abstract

The Duality of the MAPK Signaling Pathway in the Control of Metabolic Processes and Cellulase Production in Trichoderma reesei

Cited by 34 publications

References 97 publications

Transcriptomic and proteomic profiling revealed reprogramming of carbon metabolism in acetate-grown human pathogen Candida glabrata

Transcriptomic and proteomic profiling revealed reprogramming of carbon metabolism in acetate-grown human pathogen Candida glabrata

Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in Neurospora crassa

Extracellular vesicles carry cellulases in the industrial fungus Trichoderma reesei

Contact Info

Product

Resources

About