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Metagenome-assembled genome of a Chitinophaga sp. and its potential in plant biomass degradation, as well of affiliated Pandoraea and Labrys species

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Abstract

The prospection of new degrading enzymes of the plant cell wall has been the subject of many studies and is fundamental for industries, due to the great biotechnological importance of achieving a more efficient depolymerization conversion from plant polysaccharides to fermentable sugars, which are useful not only for biofuel production but also for various bioproducts. Thus, we explored the shotgun metagenome data of a bacterial community (CB10) isolated from sugarcane bagasse and recovered three metagenome-assembled genomes (MAGs). The genomic distance analyses, along with phylogenetic analysis, revealed the presence of a putative novel Chitinophaga species, a Pandoraea nosoerga, and Labrys sp. isolate. The isolation process for each one of these bacterial lineages from the community was carried out in order to relate them with the MAGs. The recovered draft genomes have reasonable completeness (72.67–100%) and contamination (0.26–2.66%) considering the respective marker lineage for Chitinophaga (Bacteroidetes), Pandoraea (Burkholderiales), and Labrys (Rhizobiales). The in-vitro assay detected cellulolytic activity (endoglucanases) only for the isolate Chitinophaga, and its genome analysis revealed 319 CAZymes, of which 115 are classified as plant cell wall degrading enzymes, which can act in fractions of hemicellulose and pectin. Our study highlights the potential of this Chitinophaga isolate provides several plant-polysaccharide-degrading enzymes.

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Data availability

The 16S rRNA gene sequences of isolates Chitinophaga sp. CB10 (CB10_01), P. nosoerga CB10 (CB10_02) and Labrys sp. CB10 (CB10_03) have been deposited in the GenBank database under accession numbers MW703979, MW703978 and MW703980, respectively. The genome sequences were deposited in GenBank database at the National Center for Biotechnology Information (NCBI) under the accession numbers: MLAV00000000 (Chitinophaga sp. CB10), NJGW00000000 (P. nosoerga CB10) and NJGX00000000 (Labrys sp. CB10). The raw data generated for this study were deposited in the NCBI - Sequence Read Archive (SRA), under BioProject ID PRJNA335650.

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Acknowledgements

The authors would like to acknowledge the Programa de Pós-Graduação em Microbiologia Agropecuária, Universidade Estadual Paulista (UNESP), Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, SP, Brazil, for the academic support. The authors thank to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarships of M.I.G.F. and L.A.L.C.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and Conselho Nacional de desenvolvimento Científico e Tecnológico (CNPq). This work also was supported by grants from the São Paulo Research Foundation (FAPESP) [Nos. 2010/17520-9 and 2016/16624-1].

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Contributions

Conceptualization: MIGF, DGP, LTK, EGML; methodology: MIGF, DGP; formal analysis: MIGF, DGP, ESGP, LALC, JCC, CCF; investigation: MIGF, DGP; writing - original draft preparation: MIGF; writing - review and editing: DGP, ESGP, LALC; JCC, CCF, LTK, LMCA, EGML; funding acquisition: EGML, LMCA; LTK; resources: EGML, LMCA; supervision: DGP, EGML.

Corresponding author

Correspondence to Eliana Gertrudes de Macedo Lemos.

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The authors declare no conflict of interest.

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Supplementary Information

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Supplementary file1 (XLSX 36 kb)

Supplementary file2 (XLSX 111 kb)

Supplementary file3 (XLSX 156 kb)

Supplementary file4 (XLSX 57 kb)

Supplementary file5 (XLSX 57 kb)

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Supplementary file6 Qualitative cellulase activity assay. Cultures grown on a plate containing Avicel (PH-101) before (a,b,c,d), and after (e,f,g,h) staining with Congo red, (a,e) Chitinophaga sp. (isolate CB10_01) (b,f) Pandoraea nosoerga (isolate CB10_02) (c,g), Labrys sp. (isolate CB10_03), and (d,h) CB10 community (EPS 63490 kb)

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Supplementary file7 Genomic location of the predicted oriC site (highlighted in black) in Chitinophaga sp. CB10 compared to the Chitinophaga pinensis DSM 2588 genome available in DoriC database. The similarities between genomes are represented by the gray bands (EPS 84 kb)

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Supplementary file8 Genomic location of the predicted oriC site (highlighted in black) in Pandoraea nosoerga CB10 compared to the Pandoraea pulmonicola DSM 16583 genome available in DoriC database. The similarities between genomes are represented by the gray bands (EPS 70 kb)

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Supplementary file9 Consensus network tree derived from Neighbor-Joining trees from genomic distances of the Chitinophaga genus (EPS 10406 kb)

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Supplementary file10 Consensus network tree derived from Neighbor-Joining trees from genomic distances of the Pandoraea genus (EPS 10724 kb)

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Funnicelli, M.I.G., Pinheiro, D.G., Gomes-Pepe, E.S. et al. Metagenome-assembled genome of a Chitinophaga sp. and its potential in plant biomass degradation, as well of affiliated Pandoraea and Labrys species. World J Microbiol Biotechnol 37, 162 (2021). https://doi.org/10.1007/s11274-021-03128-w

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