Biomass‐degrading enzymes are catabolite repressed in anaerobic gut fungi

Henske, John K.; Gilmore, Sean P.; Haitjema, Charles H.; Solomon, Kevin; O’Malley, Michelle

doi:10.1002/aic.16395

Cited by 26 publications

(18 citation statements)

References 56 publications

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“…A key disadvantage of in situ growth of fungi for pre-treatment purposes is the loss of feedstock carbohydrates to uptake, growth and cellular activity by the pretreatment microorganism, which causes a decrease in potential product yields from the receiving biofuel producing organism [ 121 ]. In addition, the accumulation of free sugars has been shown to repress the degradation of lignocellulose by anaerobic fungi [ 4 , 122 , 123 ]. If anaerobic fungi are to be used as an effective pretreatment, then a system to remove the hydrolysed sugars from the environment must be employed to limit their consumption by the fungus to what is essential for maintenance and to mitigate catabolite repression of their hydrolytic proteins.…”

Section: Emerging Opportunities For Industrial Biofuel Productionmentioning

confidence: 99%

The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production

et al. 2021

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Lignocellulose is a promising feedstock for biofuel production as a renewable, carbohydrate-rich and globally abundant source of biomass. However, challenges faced include environmental and/or financial costs associated with typical lignocellulose pretreatments needed to overcome the natural recalcitrance of the material before conversion to biofuel. Anaerobic fungi are a group of underexplored microorganisms belonging to the early diverging phylum Neocallimastigomycota and are native to the intricately evolved digestive system of mammalian herbivores. Anaerobic fungi have promising potential for application in biofuel production processes due to the combination of their highly effective ability to hydrolyse lignocellulose and capability to convert this substrate to H2 and ethanol. Furthermore, they can produce volatile fatty acid precursors for subsequent biological conversion to H2 or CH4 by other microorganisms. The complex biological characteristics of their natural habitat are described, and these features are contextualised towards the development of suitable industrial systems for in vitro growth. Moreover, progress towards achieving that goal is reviewed in terms of process and genetic engineering. In addition, emerging opportunities are presented for the use of anaerobic fungi for lignocellulose pretreatment; dark fermentation; bioethanol production; and the potential for integration with methanogenesis, microbial electrolysis cells and photofermentation.

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Section: Emerging Opportunities For Industrial Biofuel Productionmentioning

confidence: 99%

The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production

et al. 2021

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“…Isolation of AGF taxa enables taxonomic, metabolic, physiological and ultrastructural characterization of individual taxa. As well, cultures availability enables subsequent—omics, synthetic and system‐biology, and biogeography‐based investigations (Couger et al ., 2015; Seppälä et al ., 2016; Haitjema et al ., 2017; Calkins et al ., 2018; Henske et al ., 2018a; Henske et al ., 2018b; Murphy et al ., 2019), as well as evaluation of evolutionary processes underpinning speciation in the AGF (Youssef et al ., 2013; Wang et al ., 2019). However, efforts to isolate and maintain AGF strains have lagged behind their aerobic counterparts mainly due to their strict anaerobic nature and the lack of reliable long‐term storage procedures.…”

Section: Introductionmentioning

confidence: 99%

Assessing anaerobic gut fungal diversity in herbivores using D1/D2 large ribosomal subunit sequencing and multi‐year isolation

Hanafy

Johnson

Youssef

2020

Environmental Microbiology

111

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The anaerobic gut fungi (AGF, Neocallimastigomycota) reside in the alimentary tracts of herbivores where they play a central role in the breakdown of plant material. Here, we report on the development of the hypervariable domains D1/D2 of the large ribosomal subunit (D1/D2 LSU) as a barcoding marker for the AGF. We generated a reference D1/D2 LSU database for all cultured AGF genera, as well as the majority of candidate genera encountered in prior internal transcribed spacer 1 (ITS1)-based surveys. Subsequently, a D1/D2 LSUbased diversity survey using long read PacBio SMRT sequencing was conducted on faecal samples from 21 wild and domesticated herbivores. Twenty-eight genera and candidate genera were identified, including multiple novel lineages that were predominantly, but not exclusively, identified in wild herbivores. Association between certain AGF genera and animal lifestyles, or animal host family was observed. Finally, to address the current paucity of AGF isolates, concurrent isolation efforts utilizing multiple approaches to maximize recovery yielded 216 isolates belonging to 12 different genera, several of which have no prior cultured-representatives. Our results establish the utility of D1/D2 LSU and PacBio sequencing for AGF diversity surveys, the culturability of multiple AGF taxa, and demonstrate that wild herbivores represent a yet-untapped reservoir of AGF diversity.

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“…glucose), down-regulating the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. CCR has been studied mainly in ascomycete fungi (2) and has been examined at a global level in various major groups of fungi, such as recently in anaerobic gut fungi (3), but not in wood-rotting fungi, such as Dichomitus squalens.…”

Section: Introductionmentioning

confidence: 99%

Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens

Daly

Peng

Falco

et al. 2019

Appl Environ Microbiol

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The extent of carbon catabolite repression (CCR) at a global level is unknown in wood-rotting fungi, which are critical to the carbon cycle and are a source of biotechnological enzymes. CCR occurs in the presence of sufficient concentrations of easily metabolizable carbon sources (e.g., glucose) and involves downregulation of the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. We investigated this phenomenon in the white-rot fungus Dichomitus squalens using transcriptomics and exoproteomics. In D. squalens cultures, approximately 7% of genes were repressed in the presence of glucose compared to Avicel or xylan alone. The glucose-repressed genes included the essential components for utilization of plant biomass—carbohydrate-active enzyme (CAZyme) and carbon catabolic genes. The majority of polysaccharide-degrading CAZyme genes were repressed and included activities toward all major carbohydrate polymers present in plant cell walls, while repression of ligninolytic genes also occurred. The transcriptome-level repression of the CAZyme genes observed on the Avicel cultures was strongly supported by exoproteomics. Protease-encoding genes were generally not glucose repressed, indicating their likely dominant role in scavenging for nitrogen rather than carbon. The extent of CCR is surprising, given that D. squalens rarely experiences high free sugar concentrations in its woody environment, and it indicates that biotechnological use of D. squalens for modification of plant biomass would benefit from derepressed or constitutively CAZyme-expressing strains. IMPORTANCE White-rot fungi are critical to the carbon cycle because they can mineralize all wood components using enzymes that also have biotechnological potential. The occurrence of carbon catabolite repression (CCR) in white-rot fungi is poorly understood. Previously, CCR in wood-rotting fungi has only been demonstrated for a small number of genes. We demonstrated widespread glucose-mediated CCR of plant biomass utilization in the white-rot fungus Dichomitus squalens. This indicates that the CCR mechanism has been largely retained even though wood-rotting fungi rarely experience commonly considered CCR conditions in their woody environment. The general lack of repression of genes encoding proteases along with the reduction in secreted CAZymes during CCR suggested that the retention of CCR may be connected with the need to conserve nitrogen use during growth on nitrogen-scarce wood. The widespread repression indicates that derepressed strains could be beneficial for enzyme production.

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Biomass‐degrading enzymes are catabolite repressed in anaerobic gut fungi

Cited by 26 publications

References 56 publications

The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production

The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production

Assessing anaerobic gut fungal diversity in herbivores using D1/D2 large ribosomal subunit sequencing and multi‐year isolation

Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens

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