Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes

Romero Victorica, Matias; Soria, Marcelo A.; Batista-García, Ramón Alberto; Ceja-Navarro, Javier A.; Vikram, Surendra; Ortiz, Maximiliano; Ontañon, Ornella; Ghio, Silvina; Martínez-Ávila, Liliana; Quintero García, Omar Jasiel; Etcheverry, Clara; Campos, Eleonora; Cowan, Donald; Arneodo, Joel; Talia, Paola M.

doi:10.1038/s41598-020-60850-5

Title: Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes

Journal Article · Mon Mar 02 00:00:00 EST 2020 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-020-60850-5· OSTI ID:1615315

^[1];

^[2]; Batista-García, Ramón Alberto ^[3];

^[4]; Vikram, Surendra ^[5]; Ortiz, Maximiliano ^[5]; Ontañon, Ornella ^[1]; Ghio, Silvina ^[1]; Martínez-Ávila, Liliana ^[3]; Quintero García, Omar Jasiel ^[3]; Etcheverry, Clara ^[6]; Campos, Eleonora ^[1]; Cowan, Donald ^[5]; Arneodo, Joel ^[1]; Talia, Paola M. ^[1]

Consejo Nacional de investigaciones Científicas y Tecnológicas (CONICET), Hurlingham, Buenos Aires (Argentina). Inst. de Agrobiotecnología y Biología Molecular (IABIMO), Inst. Nacional de Tecnología Agropecuaria (INTA)
Univ. de Buenos Aires, Ciudad Autónoma de Buenos Aires (Argentina). Inst. de Investigaciones en Biociencias Agrícolas y Ambientales (INBA CONICET)
Univ. Autónoma del Estado Morelos, Cuernavaca, Morelos (Mexico). Centro de Investigación en Dinámica Celular, Inst. de Investigación en Ciencias Básicas y Aplicadas
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
Univ. of Pretoria, Pretoria (South Africa)
Univ. Nacional del Nordeste, Corrientes (Argentina)

In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits, Cortaritermes fulviceps and Nasutitermes aquilinus. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with C. fulviceps (a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas N. aquilinus (a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The C. fulviceps gut microbiome was enriched specifically in genes coding for debranching- and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4-xylanase, Xyl10E, was cloned and expressed in Escherichia coli. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1615315

Journal Information:: Scientific Reports, Vol. 10, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 15 works

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Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BioMed Central https://doi.org/10.14288/1.0074600	text	January 2012

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Parsing in vivo and in vitro contributions to microcrystalline cellulose hydrolysis by multidomain glycoside hydrolases in the Caldicellulosiruptor bescii secretome Conway, Jonathan M.; Crosby, James R.; McKinley, Bennett S. Biotechnology and Bioengineering, Vol. 115, Issue 10 https://doi.org/10.1002/bit.26773	journal	July 2018
Genomic and physiological analyses reveal that extremely thermophilic Caldicellulosiruptor changbaiensis deploys uncommon cellulose attachment mechanisms Khan, Asma M. A. M.; Mendoza, Carl; Hauk, Valerie J. Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10 https://doi.org/10.1007/s10295-019-02222-1	journal	August 2019
Insights into the roles of non-catalytic residues in the active site of a GH10 xylanase with activity on cellulose Chu, Yindi; Tu, Tao; Penttinen, Leena Journal of Biological Chemistry, Vol. 292, Issue 47 https://doi.org/10.1074/jbc.m117.807768	journal	October 2017
Functional Analysis of the Glucan Degradation Locus in Caldicellulosiruptor bescii Reveals Essential Roles of Component Glycoside Hydrolases in Plant Biomass Deconstruction Conway, Jonathan M.; McKinley, Bennett S.; Seals, Nathaniel L. Applied and Environmental Microbiology, Vol. 83, Issue 24 https://doi.org/10.1128/aem.01828-17	journal	October 2017
Discovery of a Thermostable GH10 Xylanase with Broad Substrate Specificity from the Arctic Mid-Ocean Ridge Vent System Fredriksen, L.; Stokke, R.; Jensen, M. S. Applied and Environmental Microbiology, Vol. 85, Issue 6 https://doi.org/10.1128/aem.02970-18	journal	March 2019
Production and Partial Characterization of an Alkaline Xylanase from a Novel Fungus Cladosporium oxysporum Guan, Guo-Qiang; Zhao, Peng-Xiang; Zhao, Jin BioMed Research International, Vol. 2016 https://doi.org/10.1155/2016/4575024	journal	January 2016
High activity CAZyme cassette for improving biomass degradation in thermophiles Brunecky, Roman; Chung, Daehwan; Sarai, Nicholas S. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1014-2	journal	February 2018
A novel thermostable GH10 xylanase with activities on a wide variety of cellulosic substrates from a xylanolytic Bacillus strain exhibiting significant synergy with commercial Celluclast 1.5 L in pretreated corn stover hydrolysis Wang, Kui; Cao, Ruoting; Wang, Meiling Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1389-8	journal	March 2019
The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan Chu, Yindi; Hao, Zhenzhen; Wang, Kaikai Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1617-2	journal	December 2019
Improvement in catalytic activity and thermostability of a GH10 xylanase and its synergistic degradation of biomass with cellulase You, Shuai; Xie, Chen; Ma, Rui Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1620-7	journal	December 2019