Characterization of 16S rRNA of the gut microbiome in long-tailed macaque (Macaca fascicularis) with spontaneous type 2 diabetes mellitus

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DOI https://doi.org/10.13057/biodiv/d241141
Issue
Vol. 24 No. 11 (2023)
Section
Articles
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This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

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PRAMESTY WULAN RAMADHANTY ♥
Program of Primatology, Graduate School, Institut Pertanian Bogor. Jl. Lodaya II No. 5, Bogor 16151, West Java, Indonesia
UUS SAEPULOH
Primate Research Center, LPPM IPB, Institut Pertanian Bogor. Jl. Lodaya II No. 5, Bogor 16151, West Java, Indonesia
IRMA HERAWATI SUPARTO
Department of Chemistry, Faculty of Mathematics and Natural Science, Institut Pertanian Bogor. Jl. Tanjung Kampus IPB Dramaga, Bogor 16680, West Java, Indonesia
HUDA SHALAHUDIN DARUSMAN
Department of Anatomy, Physiology, and Pharmacology, Faculty of Veterinary, Institut Pertanian Bogor. Jl. Agatis Kampus IPB Dramaga, Bogor 16680, West Java, Indonesia

Abstract

Abstract. Ramadhanty PW, Saepuloh U, Suparto IH, Darusman HS. 2023. Characterization of 16S rRNA of the gut microbiome in long-tailed macaque (Macaca fascicularis) with spontaneous type 2 diabetes mellitus. Biodiversitas 24: 6191-6199. The gut microbiota in the body is very complex and varied. It is known to influence human health. Imbalance (dysbiosis) of the gut microbiota can lead to type 2 diabetes mellitus (T2DM) and become a new feature in the development of the disease. Several human studies have compared the bacterial community in T2DM and non-T2DM patients. Until now, research on gut microbiota associated with T2DM in non-human primate animal models is still rare. T2DM can be developed by long-tailed macaque with clinical features similar to humans, which provides important information about the relationship between gut microbiota and T2DM. This study aims to characterize full-length 16S rRNA genes to obtain gut microbiota profiles in long-tailed macaques with and without spontaneous T2DM. The characterization was carried out using a metagenomic approach targeted at the full-length 16S rRNA gene with Nanopore technology (GridION) as one of the third-generation sequencing. The sample used was rectal swabs from adult male long-tailed macaques in the spontaneous T2DM group (n=3) and non-T2DM group (n=3). An increase in the alpha diversity, Firmicutes phylum, Oscillibacter genus, Oscillibacter valericigenes, and Oscillibacter ruminantium species, as well as a decrease in the Proteobacteria phylum were found in the T2DM group. The Firmicutes/Bacteroidetes ratio was also increased in the T2DM group compared to the non-T2DM group, which indicates dysbiosis. Based on these results, the metagenomic marker of the gut microbiome T2DM was obtained in long-tailed macaque primates, similar to humans with T2DM.

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References
Ahmad A, Yang W, Chen G, Shafiq M, Javed S, Zaidi SSA, Shahid R, Liu C, Bokhari H. 2019. Analysis of gut microbiota of obese individuals with type 2 diabetes and healthy individuals. PLoS One. 14(12):1–15. doi:10.1371/ journal.pone.0226372.
Arora A, Behl T, Sehgal A, Singh S, Sharma N, Bhatia S, Sobarzo-Sanchez E, Bungau S. 2021. Unravelling the involvement of gut microbiota in type 2 diabetes mellitus. Life Sci. 273:119311. doi:10.1016/j.lfs.2021.119311.
Berg G, Rybakova D, Fischer D, Cernava T, Vergès M-CC, Charles T, Chen X, Cocolin L, Eversole K, Corral GH, et al.. 2020. Correction to: Microbiome definition re-visited: old concepts and new challenges. Microbiome. 8(1):1–22. doi:10.1186/s40168-020-00905-x.
Bharti R, Grimm DG. 2021. Current challenges and best-practice protocols for microbiome analysis. Brief Bioinform. 22(1):178–193. doi:10.1093/bib/ bbz155.
Bhute SS, Suryavanshi M V., Joshi SM, Yajnik CS, Shouche YS, Ghaskadbi SS. 2017. Gut microbial diversity assessment of Indian type-2-diabetics reveals alterations in eubacteria, archaea, and eukaryotes. Front Microbiol. 8:1–15. doi:10.3389/fmicb.2017.00214.
Cao Y, Yao G, Sheng Y, Yang L, Wang Z, Yang Z, Zhuang P, Zhang Y. 2019. JinQi Jiangtang Tablet Regulates Gut Microbiota and Improve Insulin Sensitivity in Type 2 Diabetes Mice. J Diabetes Res. 2019. doi:10.1155/ 2019/1872134.
Chávez-Carbajal A, Pizano-Zárate ML, Hernández-Quiroz F, Ortiz-Luna GF, Morales-Hernández RM, De Sales-Millán A, Hernández-Trejo M, García-Vite A, Beltrán-Lagunes L, Hoyo-Vadillo C, et al.. 2020. Characterization of the gut microbiota of individuals at different T2D stages reveals a complex relationship with the host. Microorganisms. 8(1). doi:10.3390/microorganisms 8010094.
Curry KD, Wang Q, Nute MG, Tyshaieva A, Reeves E, Soriano S, Graeber E, Finzer P, Mendling W, Wu Q, et al.. 2021. Emu: Species-Level Microbial Community Profiling for Full-Length Nanopore 16S Reads. Nat Methods. 19(7):845-853. doi:10.1038/s41592-022-01520-4.
de Coster W, D’Hert S, Schultz DT, Crust M, van Broeckhoven C. 2018. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics. 34(15):2666-2669. doi: 10.1093/bioinformatics/bty149.
Decroli E. 2019. Diabetes Melitus Tipe 2. Padang: Pusat Penerbitan Bagian Ilmu Penyakit Dalam Fakultas Kedokteran Universitas Andalas.
Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J, et al. 2022. Microbiota in health and diseases. Signal Transduct Target Ther. 7(1):135. doi:10.1038/s41392-022-00974-4.
Huang YH, Wu YH, Tang HY, Chen ST, Wang CC, Ho WJ, Lin YH, Liu GH, Lin PY, Lo CJ, et al.. 2022. Gut Microbiota and Bile Acids Mediate the Clinical Benefits of YH1 in Male Patients with Type 2 Diabetes Mellitus: A Pilot Observational Study. Pharmaceutics. 14(9). doi:10.3390/pharmaceutics14091 857.
Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Reddy DN. 2015. Role of the normal gut microbiota. World J Gastroenterol. 21(29):8836–8847. doi:10.3748/wjg.v21.i29.8787.
Kim D, Song L, Breitwieser FP, Salzberg SL. 2016. Centrifuge: Rapid and sensitive classification of metagenomic sequences. Genome Res. doi: 10.1101/gr.210641.116.
Kleinert M, Clemmensen C, Hofmann SM, Moore MC, Renner S, Woods SC, Huypens P, Beckers J, De Angelis MH, Schürmann A, et al.. 2018. Animal models of obesity and diabetes mellitus. Nat Rev Endocrinol. 14(3):140–162. doi:10.1038/nrendo.2017.161.
Kumar B, Kinyua J, Kimotho J. 2022. Determination of microbial metagenomic markers of Type 2 Diabetes Mellitus (T2DM) in patients visiting South C Health Centre in Nairobi Kenya. J Agric Sci Technol. 21(2):83–95. doi:10.4314/jagst.v21i2.7.
Larsen N, Vogensen FK, Van Den Berg FWJ, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 5(2). doi:10.1371/journal.pone.0009085.
Li Q, Chang Y, Zhang K, Chen H, Tao S, Zhang Z. 2020. Implication of the gut microbiome composition of type 2 diabetic patients from northern China. Sci Rep. 10(1). doi:10.1038/s41598-020-62224-3.
Li X, Liang S, Xia Z, Qu J, Liu H, Liu C, Yang H, Wang J, Madsen L, Hou Y, et al.. 2018. Establishment of a Macaca fascicularis gut microbiome gene catalog and comparison with the human, pig, and mouse gut microbiomes. Gigascience. 7(9):1–10. doi:10.1093/gigascience/giy100.
Li Z, Gurung M, Rodrigues RR, Padiadpu J, Newman NK, Manes NP, Pederson JW, Greer RL, Vasquez-Perez S, You H, et al.. 2022. Microbiota and adipocyte mitochondrial damage in type 2 diabetes are linked by Mmp12+ macrophages. J Exp Med. 219(7). doi:10.1084/jem.20220017.
Matsuo Y, Komiya S, Yasumizu Y, Yasuoka Y, Mizushima K, Takagi T, Kryukov K, Fukuda A, Morimoto Y, Naito Y, et al.. 2021. Full-length 16S rRNA gene amplicon analysis of human gut microbiota using MinIONTM nanopore sequencing confers species-level resolution. BMC Microbiol. 21(35). doi:10.1186/s12866-021-02094-5.
Nuli R, Cai J, Kadeer A, Zhang Y, Mohemaiti P. 2019. Integrative analysis toward different glucose tolerance-related gut microbiota and diet. Front Endocrinol (Lausanne). doi:10.3389/fendo.2019.00295.
Nygaard AB, Tunsjø HS, Meisal R, Charnock C. 2020. A preliminary study on the potential of Nanopore MinION and Illumina MiSeq 16S rRNA gene sequencing to characterize building-dust microbiomes. Scientific Reports. 10(1):1-10. doi:10.1038/s41598-020-59771-0.
Olivares M, Schüppel V, Hassan AM, Beaumont M, Neyrinck AM, Bindels LB, Benítez-Páez A, Sanz Y, Haller D, Holzer P, et al.. 2018. The potential role of the Dipeptidyl peptidase-4-like activity from the gut microbiota on the Host Health. Front Microbiol. 9:1–10. doi:10.3389/fmicb.2018.01900.
Pickard JM, Zeng MY, Caruso R, Núñez G. 2017. Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease. Immunol Rev. 279(1):70–89. doi:10.1111/imr.12567.
Santos A, van Aerle R, Barrientos L, Martinez-Urtaza J. 2020. Computational methods for 16S metabarcoding studies using Nanopore sequencing data. Comput Struct Biotechnol J. 18:296–305. doi:10.1016/j.csbj.2020.01.005.
Sawaswong V, Praianantathavorn K, Chanchaem P, Khamwut A, Kemthong T, Hamada Y, Malaivijitnond S, Payungporn S. 2021. Comparative analysis of oral-gut microbiota between captive and wild long-tailed macaque in Thailand. Sci Rep. 11(1):1–13. doi:10.1038/s41598-021-93779-4.
Shin NR, Whon TW, Bae JW. 2015. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 33(9):496–503. doi:10.1016/ j.tibtech.2015.06.011.
Zhang X, Shen D, Fang Z, Jie Z, Qiu X, Zhang C, Chen Y, Ji L. 2013. Human Gut Microbiota Changes Reveal the Progression of Glucose Intolerance. PLoS One. 8(8). doi:10.1371/journal.pone.0071108.