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Focused Metabolism of beta-Glucans by the Soil Bacteroidetes Species Chitinophaga pinensis
KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Chemistry, Glycoscience.ORCID iD: 0000-0002-3372-8773
KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Chemistry, Glycoscience.
KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Chemistry, Glycoscience. AlbaNova Univ Ctr, KTH Royal Inst .ORCID iD: 0000-0002-8533-1022
KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Chemistry, Glycoscience.ORCID iD: 0000-0003-3572-7798
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2019 (English)In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 85, no 2, article id UNSP e02231-18Article in journal (Refereed) Published
Abstract [en]

The genome and natural habitat of Chitinophaga pinensis suggest it has the ability to degrade a wide variety of carbohydrate-based biomass. Complementing our earlier investigations into the hydrolysis of some plant polysaccharides, we now show that C. pinensis can grow directly on spruce wood and on the fungal fruiting body. Growth was stronger on fungal material, although secreted enzyme activity was high in both cases, and all biomass-induced secretomes showed a predominance of beta-glucanase activities. We therefore conducted a screen for growth on and hydrolysis of beta-glucans isolated from different sources. Most noncrystalline beta-glucans supported good growth, with variable efficiencies of polysaccharide deconstruction and oligosaccharide uptake, depending on the polysaccharide backbone linkage. In all cases, beta-glucan was the only type of polysaccharide that was effectively hydrolyzed by secreted enzymes. This contrasts with the secretion of enzymes with a broad range of activities observed during growth on complex heteroglycans. Our findings imply a role for C. pinensis in the turnover of multiple types of biomass and suggest that the species may have two metabolic modes: a "scavenging mode," where multiple different types of glycan may be degraded, and a more "focused mode" of beta-glucan metabolism. The significant accumulation of some types of beta-gluco-oligosaccharides in growth media may be due to the lack of an appropriate transport mechanism, and we propose that this is due to the specificity of expressed polysaccharide utilization loci. We present a hypothetical model for beta-glucan metabolism by C. pinensis that suggests the potential for nutrient sharing among the microbial litter community. IMPORTANCE It is well known that the forest litter layer is inhabited by a complex microbial community of bacteria and fungi. However, while the importance of fungi in the turnover of natural biomass is well established, the role of their bacterial counterparts is less extensively studied. We show that Chitinophaga pinensis, a prominent member of an important bacterial genus, is capable of using both plant and fungal biomass as a nutrient source but is particularly effective at deconstructing dead fungal material. The turnover of dead fungus is key in natural elemental cycles in the forest. We show that C. pinensis can perform extensive degradation of this material to support its own growth while also releasing sugars that may serve as nutrients for other microbial species. Our work adds detail to an increasingly complex picture of life among the environmental microbiota.

Place, publisher, year, edition, pages
AMER SOC MICROBIOLOGY , 2019. Vol. 85, no 2, article id UNSP e02231-18
Keywords [en]
beta-glucan polysaccharides, bacteria, Bacteroidetes, biomass recycling, carbohydrate active enzymes, polysaccharide utilization loci
National Category
Botany
Identifiers
URN: urn:nbn:se:kth:diva-242256DOI: 10.1128/AEM.02231-18ISI: 000455226800019PubMedID: 30413479Scopus ID: 2-s2.0-85059797944OAI: oai:DiVA.org:kth-242256DiVA, id: diva2:1284027
Note

QC 20190130

Available from: 2019-01-30 Created: 2019-01-30 Last updated: 2019-01-30Bibliographically approved

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McKee, Lauren S.Martinez-Abad, AntonioRuthes, Andrea C.Vilaplana, FranciscoBrumer, Harry

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