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The Cellulosome Paradigm in An Extreme Alkaline Environment.

ABSTRACT: Rapid decomposition of plant biomass in soda lakes is associated with microbial activity of anaerobic cellulose-degrading communities. The alkaliphilic bacterium, Clostridium alkalicellulosi, is the single known isolate from a soda lake that demonstrates cellulolytic activity. This microorganism secretes cellulolytic enzymes that degrade cellulose under anaerobic and alkaliphilic conditions. A previous study indicated that the protein fraction of cellulose-grown cultures showed similarities in composition and size to known components of the archetypical cellulosome Clostridium thermocellum. Bioinformatic analysis of the C. alkalicellulosi draft genome sequence revealed 44 cohesins, organized into 22 different scaffoldins, and 142 dockerin-containing proteins. The modular organization of the scaffoldins shared similarities to those of C. thermocellum and Acetivibrio cellulolyticus, whereas some exhibited unconventional arrangements containing peptidases and oxidative enzymes. The binding interactions among cohesins and dockerins assessed by ELISA, revealed a complex network of cellulosome assemblies and suggested both cell-associated and cell-free systems. Based on these interactions, C. alkalicellulosi cellulosomal systems have the genetic potential to create elaborate complexes, which could integrate up to 105 enzymatic subunits. The alkalistable C. alkalicellulosi cellulosomal systems and their enzymes would be amenable to biotechnological processes, such as treatment of lignocellulosic biomass following prior alkaline pretreatment.

SUBMITTER: Phitsuwan P

PROVIDER: S-EPMC6780208 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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The Cellulosome Paradigm in An Extreme Alkaline Environment.

Phitsuwan Paripok P Moraïs Sarah S Dassa Bareket B Henrissat Bernard B Bayer Edward A EA

Microorganisms 20190912 9

Rapid decomposition of plant biomass in soda lakes is associated with microbial activity of anaerobic cellulose-degrading communities. The alkaliphilic bacterium, <i>Clostridium alkalicellulosi</i>, is the single known isolate from a soda lake that demonstrates cellulolytic activity. This microorganism secretes cellulolytic enzymes that degrade cellulose under anaerobic and alkaliphilic conditions. A previous study indicated that the protein fraction of cellulose-grown cultures showed similariti ...[more]

PMID: 31547347

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Project description:Fungal ?-1,3-glucanosyltransferases are cell wall-remodeling enzymes implicated in stress response, cell wall integrity, and virulence, with most fungal genomes containing multiple members. The insect-pathogenic fungus Beauveria bassiana displays robust growth over a wide pH range (pH 4 to 10). A random insertion mutant library screening for increased sensitivity to alkaline (pH 10) growth conditions resulted in the identification and mapping of a mutant to a ?-1,3-glucanosyltransferase gene (Bbgas3). Bbgas3 expression was pH dependent and regulated by the PacC transcription factor, which activates genes in response to neutral/alkaline growth conditions. Targeted gene knockout of Bbgas3 resulted in reduced growth under alkaline conditions, with only minor effects of increased sensitivity to cell wall stress (Congo red and calcofluor white) and no significant effects on fungal sensitivity to oxidative or osmotic stress. The cell walls of ?Bbgas3 aerial conidia were thinner than those of the wild-type and complemented strains in response to alkaline conditions, and ?-1,3-glucan antibody and lectin staining revealed alterations in cell surface carbohydrate epitopes. The ?Bbgas3 mutant displayed alterations in cell wall chitin and carbohydrate content in response to alkaline pH. Insect bioassays revealed impaired virulence for the ?Bbgas3 mutant depending upon the pH of the media on which the conidia were grown and harvested. Unexpectedly, a decreased median lethal time to kill (LT50, i.e., increased virulence) was seen for the mutant using intrahemocoel injection assays using conidia grown at acidic pH (5.6). These data show that BbGas3 acts as a pH-responsive cell wall-remodeling enzyme involved in resistance to extreme pH (>9).IMPORTANCE Little is known about adaptations required for growth at high (>9) pH. Here, we show that a specific fungal membrane-remodeling ?-1,3-glucanosyltransferase gene (Bbgas3) regulated by the pH-responsive PacC transcription factor forms a critical aspect of the ability of the insect-pathogenic fungus Beauveria bassiana to grow at extreme pH. The loss of Bbgas3 resulted in a unique decreased ability to grow at high pH, with little to no effects seen with respect to other stress conditions, i.e., cell wall integrity and osmotic and oxidative stress. However, pH-dependent alternations in cell wall properties and virulence were noted for the ?Bbgas3 mutant. These data provide a mechanistic insight into the importance of the specific cell wall structure required to stabilize the cell at high pH and link it to the PacC/Pal/Rim pH-sensing and regulatory system.

Dataset Information

The Cellulosome Paradigm in An Extreme Alkaline Environment.

Publications

The Cellulosome Paradigm in An Extreme Alkaline Environment.

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