Differential transcriptomic profiling of filamentous fungus during solid-state and submerged fermentation and identification of an essential regulatory gene PoxMBF1 that directly regulated cellulase and xylanase gene expression

Zhao, Shuai; Liu, Qi; Wang, Jiu-Xiang; Liao, Xu-Zhong; Guo, Hao; Li, Chengxi; Zhang, Feng-Fei; Liao, Lusheng; Luo, Xi; Feng, Jia‐Xun

doi:10.1186/s13068-019-1445-4

Cited by 33 publications

(18 citation statements)

References 33 publications

(46 reference statements)

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“…Overall, a 10-fold cost reduction for cellulase production in solid-state fermentation compared to submerged fermentation has been estimated (Tengerdy 1996). Recently, Zhao et al (2019) performed transcriptomic profiling of the filamentous fungus Penicillium oxalicum during solid-state and submerged fermentation and demonstrated, that the expression of major cellulase genes was higher under solid state conditions, while genes involved in the citric acid cycle were downregulated.…”

Section: Cellulase Production By Aerobic Fungal Biofilmsmentioning

confidence: 99%

Impacts of biofilms on the conversion of cellulose

Brethauer

Shahab

Studer

2020

Appl Microbiol Biotechnol

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Lignocellulose is a widely available renewable carbon source and a promising feedstock for the production of various chemicals in biorefineries. However, its recalcitrant nature is a major hurdle that must be overcome to enable economic conversion processes. Deconstruction of lignocellulose is part of the global carbon cycle, and efficient microbial degradation systems have evolved that might serve as models to improve commercial conversion processes. Biofilms-matrix encased, spatially organized clusters of microbial cells and the predominating lifestyle in nature-have been recognized for their essential role in the degradation of cellulose in nature, e.g., in soils or in the digestive tracts of ruminant animals. Cellulolytic biofilms allow for a high concentration of enzymes at the boundary layer between the solid substrate and the liquid phase and the more complete capture of hydrolysis products directly at the hydrolysis site, which is energetically favorable. Furthermore, enhanced expression of genes for carbohydrate active enzymes as a response to the attachment on solid substrate has been demonstrated for cellulolytic aerobic fungi and anerobic bacteria. In natural multispecies biofilms, the vicinity of different microbial species allows the creation of efficient food webs and synergistic interactions thereby, e.g., avoiding the accumulation of inhibiting metabolites. In this review, these topics are discussed and attempts to realize the benefits of biofilms in targeted applications such as the consolidated bioprocessing of lignocellulose are highlighted. Key Points & Multispecies biofilms enable efficient lignocellulose destruction in the biosphere. & Cellulose degradation by anaerobic bacteria often occurs by monolayered biofilms. & Fungal biofilms immobilize enzymes and substrates in an external digestion system. & Surface attached cultures typically show higher expression of cellulolytic enzymes.

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Section: Cellulase Production By Aerobic Fungal Biofilmsmentioning

confidence: 99%

Impacts of biofilms on the conversion of cellulose

Brethauer

Shahab

Studer

2020

Appl Microbiol Biotechnol

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“…Recently, we compared transcriptional profiles of Penicillium oxalicum strain HP7-1 cultivated in liquid and solid media containing the same carbon source, and the results indicated that SSF elevated the expression of major cellulase genes and repressed the expression of genes involved in the citric acid cycle compared with levels in SmF cultures. Subsequently, a key regulator, P. oxalicum MBF1 (PoxMBF1), was identified, which negatively affected the production of cellulase and xylanase of P. oxalicum during SSF as well as SmF (9). However, this information is insufficient to elucidate the regulatory mechanism of cellulase and xylanase gene expression under SSF.…”

mentioning

confidence: 99%

Transcription Factor Atf1 Regulates Expression of Cellulase and Xylanase Genes during Solid-State Fermentation of Ascomycetes

Zhao

Liao

Wang

et al. 2019

Appl Environ Microbiol

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Transcriptional regulation of cellulolytic and xylolytic genes in ascomycete fungi is controlled by specific carbon sources in different external environments. Here, comparative transcriptomic analyses of Penicillium oxalicum grown on wheat bran (WB), WB plus rice straw (WR), or WB plus Avicel (WA) as the sole carbon source under solid-state fermentation (SSF) revealed that most of the differentially expressed genes (DEGs) were involved in metabolism, specifically, carbohydrate metabolism. Of the DEGs, the basic core carbohydrate-active enzyme-encoding genes which responded to the plant biomass resources were identified in P. oxalicum, and their transcriptional levels changed to various extents depending on the different carbon sources. Moreover, this study found that three deletion mutants of genes encoding putative transcription factors showed significant alterations in filter paper cellulase production compared with that of a parental P. oxalicum strain with a deletion of Ku70 (ΔPoxKu70 strain) when grown on WR under SSF. Importantly, the ΔPoxAtf1 mutant (with a deletion of P. oxalicum Atf1, also called POX03016) displayed 46.1 to 183.2% more cellulase and xylanase production than a ΔPoxKu70 mutant after 2 days of growth on WR. RNA sequencing and quantitative reverse transcription-PCR revealed that PoxAtf1 dynamically regulated the expression of major cellulase and xylanase genes under SSF. PoxAtf1 bound to the promoter regions of the key cellulase and xylanase genes in vitro. This study provides novel insights into the regulatory mechanism of fungal cellulase and xylanase gene expression under SSF. IMPORTANCE The transition to a more environmentally friendly economy encourages studies involving the high-value-added utilization of lignocellulosic biomass. Solid-state fermentation (SSF), that simulates the natural habitat of soil microorganisms, is used for a variety of applications such as biomass biorefinery. Prior to the current study, our understanding of genome-wide gene expression and of the regulation of gene expression of lignocellulose-degrading enzymes in ascomycete fungi during SSF was limited. Here, we employed RNA sequencing and genetic analyses to investigate transcriptomes of Penicillium oxalicum strain EU2101 cultured on medium containing different carbon sources and to identify and characterize transcription factors for regulating the expression of cellulase and xylanase genes during SSF. The results generated will provide novel insights into genetic engineering of filamentous fungi to further increase enzyme production.

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“…Multiple efforts have been made to improve Ac resistance and elucidated mechanisms of stress resistance in yeast [4, 20, 21]. However, little attention is paid to the relationship between Ac resistance and atg22 , a small membrane-spanning protein on vacuole of S. cerevisiae .…”

Section: Discussionmentioning

confidence: 99%

Deletion of Atg22 gene contributes to reduce programmed cell death induced by acetic acid stress in Saccharomyces cerevisiae

Dong

Wang

et al. 2019

Biotechnol Biofuels

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BackgroundProgrammed cell death (PCD) induced by acetic acid, the main by-product released during cellulosic hydrolysis, cast a cloud over lignocellulosic biofuel fermented by Saccharomyces cerevisiae and became a burning problem. Atg22p, an ignored integral membrane protein located in vacuole belongs to autophagy-related genes family; prior study recently reported that it is required for autophagic degradation and efflux of amino acids from vacuole to cytoplasm. It may alleviate the intracellular starvation of nutrition caused by Ac and increase cell tolerance. Therefore, we investigate the role of atg22 in cell death process induced by Ac in which attempt is made to discover new perspectives for better understanding of the mechanisms behind tolerance and more robust industrial strain construction.ResultsIn this study, we compared cell growth, physiological changes in the absence and presence of Atg22p under Ac exposure conditions. It is observed that disruption and overexpression of Atg22p delays and enhances acetic acid-induced PCD, respectively. The deletion of Atg22p in S. cerevisiae maintains cell wall integrity, and protects cytomembrane integrity, fluidity and permeability upon Ac stress by changing cytomembrane phospholipids, sterols and fatty acids. More interestingly, atg22 deletion increases intracellular amino acids to aid yeast cells for tackling amino acid starvation and intracellular acidification. Further, atg22 deletion upregulates series of stress response genes expression such as heat shock protein family, cell wall integrity and autophagy.ConclusionsThe findings show that Atg22p possessed the new function related to cell resistance to Ac. This may help us have a deeper understanding of PCD induced by Ac and provide a new strategy to improve Ac resistance in designing industrial yeast strains for bioethanol production during lignocellulosic biofuel fermentation.

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Differential transcriptomic profiling of filamentous fungus during solid-state and submerged fermentation and identification of an essential regulatory gene PoxMBF1 that directly regulated cellulase and xylanase gene expression

Cited by 33 publications

References 33 publications

Impacts of biofilms on the conversion of cellulose

Impacts of biofilms on the conversion of cellulose

Transcription Factor Atf1 Regulates Expression of Cellulase and Xylanase Genes during Solid-State Fermentation of Ascomycetes

Deletion of Atg22 gene contributes to reduce programmed cell death induced by acetic acid stress in Saccharomyces cerevisiae

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