Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties

Douglas Antonio Alvaredo Paixão; Geizecler Tomazetto; Victoria Ramos Sodré; Thiago A. Gonçalves; Cristiane Akemi Uchima; Fernanda Büchli; Thabata Maria Alvarez; Gabriela Felix Persinoti; Márcio José da Silva; Juliano Bragatto; Marcelo Vizoná Liberato; João Paulo L. Franco Cairo; Adriana Franco Paes Leme; Fabio Marcio Squina

doi:10.1016/j.enzmictec.2021.109820

Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties

Douglas Antonio Alvaredo Paixão
, Geizecler Tomazetto
, Victoria Ramos Sodré
, Thiago A. Gonçalves
, Cristiane Akemi Uchima
, Fernanda Büchli
, Thabata Maria Alvarez
, Gabriela Felix Persinoti
, Márcio José da Silva
, Juliano Bragatto
, Marcelo Vizoná Liberato
, João Paulo L. Franco Cairo
, Adriana Franco Paes Leme
, Fabio Marcio Squina^*

^*Corresponding author for this work

Chemistry

Research output: Contribution to journal › Article › peer-review

Abstract

Although lignocellulose is the most abundant and renewable natural resource for biofuel production, its use remains under exploration because of its highly recalcitrant structure. Its deconstruction into sugar monomers is mainly driven by carbohydrate-active enzymes (CAZymes). To develop highly efficient and fast strategies to discover biomass-degrading enzymes for biorefinery applications, an enrichment process combined with integrative omics approaches was used to identify new CAZymes. The lignocellulolytic-enriched mangrove microbial community (LignoManG) established on sugarcane bagasse (SB) was enriched with lignocellulolytic bacteria and fungi such as Proteobacteria, Bacteroidetes, Basidiomycota, and Ascomycota. These microbial communities were able to degrade up to 55 % of the total SB, indicating the production of lignocellulolytic enzymes. Metagenomic analysis revealed that the LignoManG harbors 18.042 CAZyme sequences such as of cellulases, hemicellulases, carbohydrate esterases, and lytic polysaccharide monooxygenase. Similarly, our metaproteomic analysis depicted several enzymes from distinct families of different CAZy families. Based on the LignoManG data, a xylanase (coldXynZ) was selected, amplified, cloned, expressed, and biochemically characterized. The enzyme displayed psicrofilic properties, with the highest activity at 15 °C, retaining 77 % of its activity when incubated at 0 °C. Moreover, molecular modeling in silico indicated that coldXynZ is composed of a TIM barrel, which is a typical folding found in the GH10 family, and displayed similar structural features related to cold-adapted enzymes. Collectively, the data generated in this study represent a valuable resource for lignocellulolytic enzymes with potential biotechnological applications.

Original language	English
Article number	109820
Journal	ENZYME AND MICROBIAL TECHNOLOGY
Volume	148
Early online date	14 May 2021
DOIs	https://doi.org/10.1016/j.enzmictec.2021.109820
Publication status	Published - Aug 2021

Bibliographical note

Publisher Copyright:
© 2021 Elsevier Inc.

Keywords

CAZymes
Lignocellulose degradation
Mangrove
Metagenomic
Metaproteomic
Microbial enrichment
Psicrofilic xylanase

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10.1016/j.enzmictec.2021.109820

Cite this

Paixão, D. A. A., Tomazetto, G., Sodré, V. R., Gonçalves, T. A., Uchima, C. A., Büchli, F., Alvarez, T. M., Persinoti, G. F., da Silva, M. J., Bragatto, J., Liberato, M. V., Franco Cairo, J. P. L., Leme, A. F. P., & Squina, F. M. (2021). Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties. ENZYME AND MICROBIAL TECHNOLOGY, 148, Article 109820. https://doi.org/10.1016/j.enzmictec.2021.109820

@article{5f64bfa40a074603801e22e5aa986f0f,

title = "Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties",

abstract = "Although lignocellulose is the most abundant and renewable natural resource for biofuel production, its use remains under exploration because of its highly recalcitrant structure. Its deconstruction into sugar monomers is mainly driven by carbohydrate-active enzymes (CAZymes). To develop highly efficient and fast strategies to discover biomass-degrading enzymes for biorefinery applications, an enrichment process combined with integrative omics approaches was used to identify new CAZymes. The lignocellulolytic-enriched mangrove microbial community (LignoManG) established on sugarcane bagasse (SB) was enriched with lignocellulolytic bacteria and fungi such as Proteobacteria, Bacteroidetes, Basidiomycota, and Ascomycota. These microbial communities were able to degrade up to 55 \% of the total SB, indicating the production of lignocellulolytic enzymes. Metagenomic analysis revealed that the LignoManG harbors 18.042 CAZyme sequences such as of cellulases, hemicellulases, carbohydrate esterases, and lytic polysaccharide monooxygenase. Similarly, our metaproteomic analysis depicted several enzymes from distinct families of different CAZy families. Based on the LignoManG data, a xylanase (coldXynZ) was selected, amplified, cloned, expressed, and biochemically characterized. The enzyme displayed psicrofilic properties, with the highest activity at 15 °C, retaining 77 \% of its activity when incubated at 0 °C. Moreover, molecular modeling in silico indicated that coldXynZ is composed of a TIM barrel, which is a typical folding found in the GH10 family, and displayed similar structural features related to cold-adapted enzymes. Collectively, the data generated in this study represent a valuable resource for lignocellulolytic enzymes with potential biotechnological applications.",

keywords = "CAZymes, Lignocellulose degradation, Mangrove, Metagenomic, Metaproteomic, Microbial enrichment, Psicrofilic xylanase",

author = "Paix{\~a}o, \{Douglas Antonio Alvaredo\} and Geizecler Tomazetto and Sodr{\'e}, \{Victoria Ramos\} and Gon{\c c}alves, \{Thiago A.\} and Uchima, \{Cristiane Akemi\} and Fernanda B{\"u}chli and Alvarez, \{Thabata Maria\} and Persinoti, \{Gabriela Felix\} and \{da Silva\}, \{M{\'a}rcio Jos{\'e}\} and Juliano Bragatto and Liberato, \{Marcelo Vizon{\'a}\} and \{Franco Cairo\}, \{Jo{\~a}o Paulo L.\} and Leme, \{Adriana Franco Paes\} and Squina, \{Fabio Marcio\}",

note = "Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

year = "2021",

month = aug,

doi = "10.1016/j.enzmictec.2021.109820",

language = "English",

volume = "148",

journal = "ENZYME AND MICROBIAL TECHNOLOGY",

issn = "0141-0229",

publisher = "Elsevier Inc.",

}

Paixão, DAA, Tomazetto, G, Sodré, VR, Gonçalves, TA, Uchima, CA, Büchli, F, Alvarez, TM, Persinoti, GF, da Silva, MJ, Bragatto, J, Liberato, MV, Franco Cairo, JPL, Leme, AFP & Squina, FM 2021, 'Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties', ENZYME AND MICROBIAL TECHNOLOGY, vol. 148, 109820. https://doi.org/10.1016/j.enzmictec.2021.109820

TY - JOUR

T1 - Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties

AU - Paixão, Douglas Antonio Alvaredo

AU - Tomazetto, Geizecler

AU - Sodré, Victoria Ramos

AU - Gonçalves, Thiago A.

AU - Uchima, Cristiane Akemi

AU - Büchli, Fernanda

AU - Alvarez, Thabata Maria

AU - Persinoti, Gabriela Felix

AU - da Silva, Márcio José

AU - Bragatto, Juliano

AU - Liberato, Marcelo Vizoná

AU - Franco Cairo, João Paulo L.

AU - Leme, Adriana Franco Paes

AU - Squina, Fabio Marcio

PY - 2021/8

Y1 - 2021/8

N2 - Although lignocellulose is the most abundant and renewable natural resource for biofuel production, its use remains under exploration because of its highly recalcitrant structure. Its deconstruction into sugar monomers is mainly driven by carbohydrate-active enzymes (CAZymes). To develop highly efficient and fast strategies to discover biomass-degrading enzymes for biorefinery applications, an enrichment process combined with integrative omics approaches was used to identify new CAZymes. The lignocellulolytic-enriched mangrove microbial community (LignoManG) established on sugarcane bagasse (SB) was enriched with lignocellulolytic bacteria and fungi such as Proteobacteria, Bacteroidetes, Basidiomycota, and Ascomycota. These microbial communities were able to degrade up to 55 % of the total SB, indicating the production of lignocellulolytic enzymes. Metagenomic analysis revealed that the LignoManG harbors 18.042 CAZyme sequences such as of cellulases, hemicellulases, carbohydrate esterases, and lytic polysaccharide monooxygenase. Similarly, our metaproteomic analysis depicted several enzymes from distinct families of different CAZy families. Based on the LignoManG data, a xylanase (coldXynZ) was selected, amplified, cloned, expressed, and biochemically characterized. The enzyme displayed psicrofilic properties, with the highest activity at 15 °C, retaining 77 % of its activity when incubated at 0 °C. Moreover, molecular modeling in silico indicated that coldXynZ is composed of a TIM barrel, which is a typical folding found in the GH10 family, and displayed similar structural features related to cold-adapted enzymes. Collectively, the data generated in this study represent a valuable resource for lignocellulolytic enzymes with potential biotechnological applications.

AB - Although lignocellulose is the most abundant and renewable natural resource for biofuel production, its use remains under exploration because of its highly recalcitrant structure. Its deconstruction into sugar monomers is mainly driven by carbohydrate-active enzymes (CAZymes). To develop highly efficient and fast strategies to discover biomass-degrading enzymes for biorefinery applications, an enrichment process combined with integrative omics approaches was used to identify new CAZymes. The lignocellulolytic-enriched mangrove microbial community (LignoManG) established on sugarcane bagasse (SB) was enriched with lignocellulolytic bacteria and fungi such as Proteobacteria, Bacteroidetes, Basidiomycota, and Ascomycota. These microbial communities were able to degrade up to 55 % of the total SB, indicating the production of lignocellulolytic enzymes. Metagenomic analysis revealed that the LignoManG harbors 18.042 CAZyme sequences such as of cellulases, hemicellulases, carbohydrate esterases, and lytic polysaccharide monooxygenase. Similarly, our metaproteomic analysis depicted several enzymes from distinct families of different CAZy families. Based on the LignoManG data, a xylanase (coldXynZ) was selected, amplified, cloned, expressed, and biochemically characterized. The enzyme displayed psicrofilic properties, with the highest activity at 15 °C, retaining 77 % of its activity when incubated at 0 °C. Moreover, molecular modeling in silico indicated that coldXynZ is composed of a TIM barrel, which is a typical folding found in the GH10 family, and displayed similar structural features related to cold-adapted enzymes. Collectively, the data generated in this study represent a valuable resource for lignocellulolytic enzymes with potential biotechnological applications.

KW - CAZymes

KW - Lignocellulose degradation

KW - Mangrove

KW - Metagenomic

KW - Metaproteomic

KW - Microbial enrichment

KW - Psicrofilic xylanase

UR - https://www.scopus.com/pages/publications/85105704679

U2 - 10.1016/j.enzmictec.2021.109820

DO - 10.1016/j.enzmictec.2021.109820

M3 - Article

C2 - 34116762

AN - SCOPUS:85105704679

SN - 0141-0229

VL - 148

JO - ENZYME AND MICROBIAL TECHNOLOGY

JF - ENZYME AND MICROBIAL TECHNOLOGY

M1 - 109820

ER -

Microbial enrichment and meta-omics analysis identify CAZymes from mangrove sediments with unique properties

Abstract

Bibliographical note

Keywords

Access to Document

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