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Metagenomic analysis of the fecal microbiome of an adult elephant reveals the diversity of CAZymes related to lignocellulosic biomass degradation

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Abstract

The resident microbial population responsible for lignocellulosic biomass assimilation in the gastrointestinal tract of animals is a rich source for discovering novel biocatalysts finding application in the production of value-added commodities. Herbivorous animals, such as elephants, consume a variety of lignocellulosic materials in bulk amounts to support their high energy requirements. Since the interdependence of host diet and its microbiome is well established, it is necessary to explore the potential resident microbes of obligate herbivores like elephants belonging to different age classes and habitats for mining enzymes involved in complex biomass deconstruction. In the present study, metagenomic analysis of an adult elephant fecal sample using whole-genome shotgun library preparation indicated the dominant representation of microbes belonging to the phylum Proteobacteria. Subsystem- and KEGG-based analyses revealed a high potential for carbohydrate metabolism and membrane transport. CAZy database analysis identified ~55,000 ORFs that had either catalytic domains or carbohydrate-binding modules (CBMs) in the metagenomic data set. Moreover, CBMs and carbohydrate-active enzymes (CAZymes), such as glycoside hydrolases (GHs), glycosyltransferases (GTs), carbohydrate esterases (CEs) were most abundant in microbes of phylum Proteobacteria, and among them, the majority of GHs and GTs were from Bacillus subtilis and Escherichia coli. A comparative GH analysis with other gut metagenomic datasets of herbivorous animals revealed the presence of several unique GHs of the β-glucosidase, endoglucanase, and exoglucanase families thus providing a comprehensive understanding of the diverse CAZymes present in the gut microbiome of an adult elephant.

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Acknowledgements

We are thankful to National Zoological Park, New Delhi, India, for providing elephant fecal samples. NAG acknowledges ICGEB, New Delhi and Department of Biotechnology (DBT), Government of India for financial support (Grant No.: BT/PB/Centre/03/ICGEB/2011-PhaseII).

Funding

This work was supported in part by DST Ramanujan Fellowship grant (SR/S2/RJN-07/2012) and DBT grant (BT/PR10684/PBD/26/403/2013).

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Contributions

NAG and JS1 contributed to the initial design of the research. JS1 and SJ conducted the experiments, and MV and JS1 performed the bioinformatics analyses with guidance from DG, MK and NAG. The initial draft of the manuscript was prepared by NAG, JS1, FM and MV, scientific assistance and correction was done by JS2 and all the authors contributed to the subsequent stages of manuscript preparation.

Corresponding authors

Correspondence to Manoj Kumar or Naseem A. Gaur.

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The authors declare that they have no competing interests.

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Jakeer, S., Varma, M., Sharma, J. et al. Metagenomic analysis of the fecal microbiome of an adult elephant reveals the diversity of CAZymes related to lignocellulosic biomass degradation. Symbiosis 81, 209–222 (2020). https://doi.org/10.1007/s13199-020-00695-8

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