Hydrolytic Capabilities as a Key to Environmental Success: Chitinolytic and Cellulolytic Acidobacteria From Acidic Sub-arctic Soils and Boreal Peatlands

Abstract

Members of the Acidobacteria are among the most efficient colonizers of acidic terrestrial habitats but the key traits underlying their environmental fitness remain to be understood. We analyzed indigenous assemblages of Acidobacteria in a lichen-covered acidic (pH 4.1) soil of forested tundra dominated by uncultivated members of subdivision 1. An isolate of these bacteria with cells occurring within saccular chambers, strain SBC82T, was obtained. The genome of strain SBC82T consists of a 7.11-Mb chromosome and four megaplasmids, and encodes a wide repertoire of enzymes involved in degradation of chitin, cellulose, and xylan. Among those, four secreted chitinases affiliated with the glycoside hydrolase family GH18 were identified. Strain SBC82T utilized amorphous chitin as a source of carbon and nitrogen; the respective enzyme activities were detected in tests with synthetic substrates. Chitinolytic capability was also confirmed for another phylogenetically related acidobacterium isolated from a Sphagnum peat bog, strain CCO287. As revealed by metatranscriptomic analysis of chitin-amended peat, 16S rRNA reads from these acidobacteria increased in response to chitin availability. Strains SBC82T and CCO287 were assigned to a novel genus and species, Acidisarcina polymorpha gen. nov., sp. nov. Members of this genus colonize acidic soils and peatlands and specialize in degrading complex polysaccharides.

Acidobacteria are active and abundant members of diverse atmospheric H2-oxidizing communities detected in temperate soils

“…S8), including members from subdivisions 1 (genera Acidipila, Edaphobacter and Granulicella), 2 (MAGs only), 3 (genera Bryobacter, 'Candidatus Solibacter') and 4 (genus Pyrinomonas). The acidobacterial hhyL sequences stemming from pure cultures [56,57,[60][61][62][63], genomes and MAGs originated from soil (Table S4) and formed a distinct cluster (Fig. 3), as also observed with our derived amplicon sequences (Fig.…”

Recent Understanding of Soil Acidobacteria and Their Ecological Significance: A Critical Review

“…Each bacterium carries its enzyme machinery catalyzing the breakdown of diverse carbohydrates and nitrogen-containing compounds, which could be used as an identifying characteristic for differentiating varied bacterial species. Acidobacterial genomes possess genes encoding enzymes for the degradation of complex carbohydrate polymers viz., xylan, cellulose, hemicelluloses, pectin, starch, and chitin; amino acids, alcohols, and metabolic intermediates (Ward et al, 2009;Belova et al, 2018). In addition to these, gene modules for diverse carbohydrate breakdown, utilization, and biosynthesis within carbohydrate-active enzymes (CAZy) family are also present (Männistö et al, 2012;Rawat et al, 2012a), spanning across 131 glycoside hydrolase (GH) families (Gilbert, 2010).…”

“…Involvement in carbon cycle King and Weber, 2007;Banerjee et al, 2016;García-Fraile et al, 2016;Belova et al, 2018;Dedysh and Damsté, 2018 Involvement in nitrogen cycle Ward et al, 2009;Rajeev et al, 2015;Eichorst et al, 2018 Involvement in sulfur cycle Wasmund et al, 2017;Hausmann et al, 2018 Involvement in plant growth promotion Kielak et al, 2016b;Kalam et al, 2017a Involvement as "keystone taxa" Banerjee et al, 2016;Jiang et al, 2017;Li et al, 2017;Banerjee et al, 2018 Involvement in soil matrix formation Kielak et al, 2016a;Kielak et al, 2017 Establishment of biofilms Ward et al, 2009;Kielak et al, 2016a;Kielak et al, 2016b Production of exopolysaccharides Ward et al, 2009;Rawat et al, 2012a;Kielak et al, 2017 Biosynthesis of secondary metabolites Ward et al, 2009;Parsley et al, 2011;Hadjithomas et al, 2015;Damsté et al, 2017;Crits-Christoph et al, 2018 Tolerance to stress, starvation, and acidity Ward et al, 2009;Challacombe et al, 2011;Morris and Schmidt, 2013;Greening et al, 2015;Rajeev et al, 2015;Eichorst et al, 2018;Domeignoz-Horta et al, 2019;Pinto et al, 2020 Presence of mobile genetic elements Frost et al, 2005;…”

“…Genomic studies highlight the carbohydrate utilization potential exhibited by Acidobacteria members (Ward et al, 2009;Kielak et al, 2016a). The presence of genes encoding enzymes for the degradation of complex carbohydrate polymers like cellulose, hemicellulose, chitin, xylan, and lignin derivatives signifies their active participation in the carbon circuit as decomposers in soil (Ward et al, 2009;Wegner and Liesack, 2017;Banerjee et al, 2018;Belova et al, 2018) and cycling of organic matter derived from plants, fungi, and insects (King and Weber, 2007;García-Fraile et al, 2016;Dedysh and Damsté, 2018).…”

Closely Located but Totally Distinct: Highly Contrasting Prokaryotic Diversity Patterns in Raised Bogs and Eutrophic Fens

“…Thus, most acidobacteria that are commonly detected in bogs are affiliated with one particular class of this phylum, i.e., the Acidobacteriia [36]. The latter accommodates aerobic and facultatively anaerobic, acidophilic or acidotolerant, mesophilic and psychrotolerant, chemoheterotrophic bacteria, which utilize various sugars and polysaccharides, and possess a number of hydrolytic capabilities including the abilities to degrade cellulose and chitin [37,38]. The most abundant bog-specific OTU determined in our study belonged to the as-yet-uncultivated group within the order Acidobacteriales and displayed highest similarity to the environmental clone sequence (GenBank accession No.…”