Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases
Identifieur interne : 000178 ( Pmc/Curation ); précédent : 000177; suivant : 000179Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases
Auteurs : Adam J. Book [États-Unis] ; Ragothaman M. Yennamalli [États-Unis] ; Taichi E. Takasuka [États-Unis] ; Cameron R. Currie [États-Unis] ; George N. Phillips [États-Unis] ; Brian G. Fox [États-Unis]Source :
- Biotechnology for Biofuels [ 1754-6834 ] ; 2014.
Abstract
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.
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.
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.
The online version of this article (doi:10.1186/1754-6834-7-109) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/1754-6834-7-109
PubMed: 25161697
PubMed Central: 4144037
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<series><title level="j">Biotechnology for Biofuels</title>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>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.</p>
</sec>
<sec><title>Results</title>
<p>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.</p>
</sec>
<sec><title>Conclusions</title>
<p>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.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/1754-6834-7-109) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Biotechnol Biofuels</journal-id>
<journal-id journal-id-type="iso-abbrev">Biotechnol Biofuels</journal-id>
<journal-title-group><journal-title>Biotechnology for Biofuels</journal-title>
</journal-title-group>
<issn pub-type="epub">1754-6834</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25161697</article-id>
<article-id pub-id-type="pmc">4144037</article-id>
<article-id pub-id-type="publisher-id">512</article-id>
<article-id pub-id-type="doi">10.1186/1754-6834-7-109</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Book</surname>
<given-names>Adam J</given-names>
</name>
<address><email>ajbook@wisc.edu</email>
</address>
<xref ref-type="aff" rid="Aff49"></xref>
<xref ref-type="aff" rid="Aff50"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Yennamalli</surname>
<given-names>Ragothaman M</given-names>
</name>
<address><email>ragothaman@rice.edu</email>
</address>
<xref ref-type="aff" rid="Aff51"></xref>
<xref ref-type="aff" rid="Aff52"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Takasuka</surname>
<given-names>Taichi E</given-names>
</name>
<address><email>ttakasuka@glbrc.wisc.edu</email>
</address>
<xref ref-type="aff" rid="Aff49"></xref>
<xref ref-type="aff" rid="Aff51"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Currie</surname>
<given-names>Cameron R</given-names>
</name>
<address><email>currie@bact.wisc.edu</email>
</address>
<xref ref-type="aff" rid="Aff49"></xref>
<xref ref-type="aff" rid="Aff50"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Phillips</surname>
<given-names>George N</given-names>
<suffix>Jr</suffix>
</name>
<address><email>georgep@rice.edu</email>
</address>
<xref ref-type="aff" rid="Aff49"></xref>
<xref ref-type="aff" rid="Aff51"></xref>
<xref ref-type="aff" rid="Aff52"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Fox</surname>
<given-names>Brian G</given-names>
</name>
<address><email>bgfox@biochem.wisc.edu</email>
</address>
<xref ref-type="aff" rid="Aff49"></xref>
<xref ref-type="aff" rid="Aff51"></xref>
</contrib>
<aff id="Aff49"><label></label>
Department of Energy, Great Lakes Bioenergy Research Center, Madison, 1552 University Avenue, Madison, WI 53726 USA</aff>
<aff id="Aff50"><label></label>
Department of Bacteriology, University of Wisconsin-Madison, Microbial Sciences Building, 1550 Linden Dr., Madison, WI 53706 USA</aff>
<aff id="Aff51"><label></label>
Department of Biochemistry, University of Wisconsin-Madison, Biochemistry Addition, 433 Babcock Dr., Madison, WI 53706 USA</aff>
<aff id="Aff52"><label></label>
Biosciences at Rice, Rice University, George R. Brown Hall, Houston, TX 77005 USA</aff>
</contrib-group>
<pub-date pub-type="epub"><day>6</day>
<month>8</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<volume>7</volume>
<elocation-id>109</elocation-id>
<history><date date-type="received"><day>14</day>
<month>3</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>7</day>
<month>7</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© Book et al.; licensee BioMed Central Ltd. 2014</copyright-statement>
<license license-type="open-access"><license-p>This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">http://creativecommons.org/licenses/by/4.0</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1"><sec><title>Background</title>
<p>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.</p>
</sec>
<sec><title>Results</title>
<p>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.</p>
</sec>
<sec><title>Conclusions</title>
<p>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.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/1754-6834-7-109) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<kwd-group xml:lang="en"><title>Keywords</title>
<kwd>Lytic polysaccharide monooxygenase</kwd>
<kwd>LPMO</kwd>
<kwd>Cellulase</kwd>
<kwd>Chitinase</kwd>
<kwd>Streptomyces</kwd>
<kwd>AA9</kwd>
<kwd>AA10</kwd>
<kwd>Enzyme evolution</kwd>
<kwd>Biofuels</kwd>
</kwd-group>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2014</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>
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