Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

Book, Adam J.; Yennamalli, Ragothaman M.; Takasuka, Taichi E.; Currie, Cameron R.; Phillips, George N.; Fox, Brian G.

doi:10.1186/1754-6834-7-109

Title: Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

Journal Article · Wed Aug 06 00:00:00 EDT 2014 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/1754-6834-7-109· OSTI ID:1626659

Book, Adam J. ^[1]; Yennamalli, Ragothaman M. ^[2]; Takasuka, Taichi E. ^[3]; Currie, Cameron R. ^[1]; Phillips, George N. ^[4]; Fox, Brian G. ^[3]

Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Biochemistry Addition
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Biochemistry Addition

Background: Understanding the diversity of lignocellulose-degrading enzymes in nature will provide insights for the improvement of cellulolytic enzyme cocktails used in the biofuels industry. Two families of enzymes, fungal AA9 and bacterial AA10, have recently been characterized as crystalline cellulose or chitin-cleaving lytic polysaccharide monooxygenases (LPMOs). Here we analyze the sequences, structures, and evolution of LPMOs to understand the factors that may influence substrate specificity both within and between these enzyme families. Results: Comparative analysis of sequences, solved structures, and homology models from AA9 and AA10 LPMO families demonstrated that, although these two LPMO families are highly conserved, structurally they have minimal sequence similarity outside the active site residues. Phylogenetic analysis of the AA10 family identified clades with putative chitinolytic and cellulolytic activities. Estimation of the rate of synonymous versus non-synonymous substitutions (dN/dS) within two major AA10 subclades showed distinct selective pressures between putative cellulolytic genes (subclade A) and CBP21-like chitinolytic genes (subclade D). Estimation of site-specific selection demonstrated that changes in the active sites were strongly negatively selected in all subclades. Furthermore, all codons in the subclade D had dN/dS values of less than 0.7, whereas codons in the cellulolytic subclade had dN/dS values of greater than 1.5. Positively selected codons were enriched at sites localized on the surface of the protein adjacent to the active site. Conclusions: The structural similarity but absence of significant sequence similarity between AA9 and AA10 families suggests that these enzyme families share an ancient ancestral protein. Combined analysis of amino acid sites under Darwinian selection and structural homology modeling identified a subclade of AA10 with diversifying selection at different surfaces, potentially used for cellulose-binding and protein-protein interactions. Together, these data indicate that AA10 LPMOs are under selection to change their function, which may optimize cellulolytic activity. This work provides a phylogenetic basis for identifying and classifying additional cellulolytic or chitinolytic LPMOs.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FC02-07ER64494; FG02-04ER25627

OSTI ID:: 1626659

Journal Information:: Biotechnology for Biofuels, Vol. 7, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Title: Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

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