The Gut Microbiomes of Wild Rodents within Forested Environments in Sarawak, Borneo

Rodent Gut Microbiomes in Sarawak Forests

Authors

  • MUHAMMAD AMIN IMAN AZMI Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • JULIUS WILLIAM-DEE Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • MUHD AMSYARI MORNI Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia; Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • NUR AFIQAH AQILAH AZHAR Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • NOR AL-SHUHADAH SABARUDIN Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • EMY RITTA JINGGONG Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • SYAMZURAINI ZOLKAPLEY Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • CHENG-SIANG TAN Centre for Tropical and Emerging Diseases, Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia
  • FAISAL ALI ANWARALI KHAN Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia

DOI:

https://doi.org/10.33736/bjrst.7517.2024

Abstract

The gut microbiota of rodents is shaped by highly diverse bacterial communities. Within the gut environment, there are core gut bacteria that are responsible for facilitating essential bodily processes while maintaining the health of the host rodents. Currently, research on the gut microbiota of wild rodents in Borneo remains limited, especially those encompassing the potential influence of environmental factors. Through the Next-Generation Sequencing (NGS) performed using Oxford Nanopore Technologies, a total of 1052 bacterial genera were detected from 16 rodent individuals of six rodent species. These bacteria were found to be prevalent in the gut microbiota of wild rodents in forested regions. Several bacterial families of importance belonging to the phylum Bacillota were identified, including Lachnospiraceae (18%), Lactobacillaceae (20%) and Oscillospiraceae (19%). They were found to have a high relative abundance when compared with other bacterial families. The diversity of gut microbes among individual rodents showed no significant differences. However, the gut microbiome composition of wild rodents appears to have been influenced by the host species and their life stages. The outcome of this study allows for a better understanding of the prevailing core microbiome members shared across multiple wild rodent individuals within forested areas.

References

Anders, J.L., Moustafa, M.A.M., Mohamed, W.M.A., Hayakawa, T., Nakao, R., & Koizumi, I. (2021). Comparing the gut microbiome along the gastrointestinal tract of three sympatric species of wild rodents. Scientific Reports, 11(1), 19929. DOI:10.1038/s41598-021-99379-6

Archie, E.A., & Tung, J. (2015). Social behavior and the microbiome. Current Opinion in Behavioral Sciences, 6: 28-34. DOI: 10.1016/j.cobeha.2015.07.008

Bäumler, A.J., & Sperandio, V. (2016). Interactions between the microbiota and pathogenic bacteria in the gut. Nature, 535(7610): 85-93. DOI:10.1038/nature18849

Bickham, J.W., Wood, C.C., & Patton, J.C. (1995). Biogeographic implications of cytochrome b sequences and allozymes in sockeye (Oncorhynchus nerka). Journal of Heredity, 86(2): 140-144. DOI:10.1093/oxfordjournals.jhered.a111544

Biddle, A., Stewart, L., Blanchard, J., & Leschine, S. (2013). Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity, 5(3): 627-640. DOI:10.3390/d5030627

Campbell, J.H., Foster, C.M., Vishnivetskaya, T., Campbell, A.G., Yang, Z.K., Wymore, A., Palumbo, A.V., Chesler, E.J., & Podar, M. (2012). Host genetic and environmental effects on mouse intestinal microbiota. The ISME Journal, 6(11): 2033-2044. DOI:10.1038/ismej.2012.54

Carlson, CJ., Kracalik, I.T., Ross, N., Alexander, K.A., Hugh-Jones, M.E., Fegan, M., Elkin B.T., Epp, T., Shury, T.K., Zhang, W., Bagirova, M., Getz, W.M., & Blackburn, J.K. (2019). The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife. Nature Microbiology, 4(8), 1337-1343. DOI:10.1038/s41564-019-0435-4

Coyte, K.Z., & Rakoff-Nahoum, S. (2019). Understanding competition and cooperation within the mammalian gut microbiome. Current Biology, 29(11): R538-R544. DOI:10.1016/j.cub.2019.04.017

Erickson, M.C. (2016). Overview: Foodborne pathogens in wildlife populations. In: Jay-Russell, M., & Doyle, M.P. (eds.), Food Safety Risks from Wildlife: Challenges in Agriculture, Conservation, and Public Health. Cham: Springer. pp. 1-30. DOI:10.1007/978-3-319-24442-6_1

Euzéby, J. (2010). List of new names and new combinations previously effectively, but not validly, published. International Journal of Systematic and Evolutionary Microbiology, 60(3): 469-472. DOI:10.1099/ijs.0.022855-0

Fagre, A.C., Cohen, L.E., Eskew, E.A., Farrell, M., Glennon, E., Joseph, M.B., Frank, H.K., Ryan, S.J., Carlson, C.J., & Albery, G.F. (2022). Assessing the risk of human‐to‐wildlife pathogen transmission for conservation and public health. Ecology Letters, 25(6), 1534-1549. DOI:10.1111/ele.14003

Fan, C., Zhang, L., Jia, S., Tang, X., Fu, H., Li, W., Liu, C., Zhang, H., Cheng, Q., & Zhang, Y. (2022). Seasonal variations in the composition and functional profiles of gut microbiota reflect dietary changes in plateau pikas. Integrative Zoology, 17(3): 379-395. DOI:10.1111/1749-4877.12630

Fenn, J., Taylor, C., Goertz, S., Wanelik, K.M., Paterson, S., Begon, M., Jackson, J., & Bradley, J. (2023). Discrete patterns of microbiome variability across timescales in a wild rodent population. BMC Microbiology, 23(1): 1-17. DOI:10.1186/s12866-023-02824-x

Gani, M., Mohd-Ridwan, A.R., Sitam, F.T., Kamarudin, Z., Selamat, S.S., Awang, N.M.Z., Karuppannan, K.V., & Md-Zain, B. M. (2024). Habitat shapes the gut microbiome diversity of Malayan tigers (Panthera tigris jacksoni) as revealed through metabarcoding 16S rRNA profiling. World Journal of Microbiology and Biotechnology, 40(4), 111. DOI:10.1007/s11274-023-03868-x

Hou, K., Wu, Z.X., Chen, X.Y., Wang, J.Q., Zhang, D., Xiao, C., Zhu, D., Koya, J.B., Wei, L., Li, J., & Chen, Z.S. (2022). Microbiota in health and diseases. Signal Transduction and Targeted Therapy, 7(1): 135. DOI:10.1038/s41392-022-00974-4

Jahan, N.A., Lindsey, L.L., Kipp, E.J., Reinschmidt, A., Heins, B.J., Runck, A.M., & Larsen, P.A. (2021). Nanopore-based surveillance of zoonotic bacterial pathogens in farm dwelling peridomestic rodents. Pathogens, 10(9): 1183. DOI:10.3390/pathogens10091183

Jose, L., Lee, W., Hanya, G., Tuuga, A., Goossens, B., Tangah, J., Matsuda, I., & Kumar, V.S. (2024). Gut microbial community in proboscis monkeys (Nasalis larvatus): Implications for effects of geographical and social factors. Royal Society Open Science, 11(7), 231756. DOI:10.1098/rsos.231756

Kerfeld, C.A., & Scott, K.M. (2011). Using BLAST to teach “E-value-tionary” concepts. PLoS Biology, 9(2): e1001014. DOI:10.1371/journal.pbio.1001014

Khairulmunir, M., Gani, M., Karuppannan, K.V., Mohd-Ridwan, A.R., & Md-Zain, B.M. (2023). High-throughput DNA metabarcoding for determining the gut microbiome of captive critically endangered Malayan tiger (Pantheratigrisjacksoni) during fasting. Biodiversity Data Journal, 11, e104757. DOI:10.3897/BDJ.11.e104757

Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111-120. DOI:10.1007/BF01731581

Kinross, J.M., Darzi, A.W., & Nicholson, J.K. (2011). Gut microbiome-host interactions in health and disease. Genome Medicine, 3: 1-12. DOI:10.1186/gm228

Kohl, K.D., Dieppa-Colón, E., Goyco-Blas, J., Peralta-Martínez, K., Scafidi, L., Shah, S., Zawacki, E., Barts, N., Ahn, Y., Hedayati, S., Secor, S.M., & Rowe, M.P. (2022). Gut microbial ecology of five species of sympatric desert rodents in relation to herbivorous and insectivorous feeding strategies. Integrative and Comparative Biology, 62(2): 237-251. DOI:10.1093/icb/icac045

König, H., & Fröhlich, J. (2017). Lactic acid bacteria. In: Konig, H., Unden, G., & Frohlich, J. (eds.), Biology of Microorganisms on Grape, in Must and in Wine. Cham: Springer. pp. 3-41. DOI:10.1007/978-3-319-60021-5

Leser, T.D., & Mølbak, L. (2009). Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environmental Microbiology, 11(9): 2194-2206. DOI:10.1111/j.1462-2920.2009.01941.x

Liu, X., Mao, B., Gu, J., Wu, J., Cui, S., Wang, G., Zhao, J., Zhang, J., & Chen, W. (2021). Blautia—a new functional genus with potential probiotic properties? Gut Microbes, 13(1): 1875796. DOI:10.1080/19490976.2021.1875796

Lobato-Bailón, L., García-Ulloa, M., Santos, A., Guixé, D., Camprodon, J., Florensa-Rius, X., Molleda, R., Manzano, R., Ribas, M.P., Espunyes, J., Dias-Alves, A., Marco, I., Migura-Garcia, L., & Martínez-Urtaza, J. (2023). The fecal bacterial microbiome of the Kuhl’s pipistrelle bat (Pipistrellus kuhlii) reflects landscape anthropogenic pressure. Animal Microbiome, 5(1): 1-14. DOI:10.1186/s42523-023-00229-9

Maurice, C.F., Knowles, S.C., Ladau, J., Pollard, K.S., Fenton, A., Pedersen, A.B., & Turnbaugh, P.J. (2015). Marked seasonal variation in the wild mouse gut microbiota. The ISME Journal, 9(11): 2423-2434. DOI:10.1038/ismej.2015.53

McMurdie, P.J., & Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PloS ONE, 8(4): e61217. DOI:10.1371/journal.pone.0061217

Mohd-Yusof, N.S., Abdul-Latiff, M.A.B., Badrulisham, A.S., Othman, N., Yaakop, S., Md-Nor, S., & Md-Zain, B.M. (2022). First report on metabarcoding analysis of gut microbiome in Island Flying Fox (Pteropus hypomelanus) in island populations of Malaysia. Biodiversity Data Journal, 10, e69631. DOI:10.3897/BDJ.10.e69631

Payne, J., Francis, C.M., & Phllipps, K. (1985). A field guide to the mammals of Borneo. Kota Kinabalu: The Sabah Society.

Perlman, D., Martínez-Álvaro, M., Moraïs, S., Altshuler, I., Hagen, L.H., Jami, E., Roehe, R., Pope, P.B., & Mizrahi, I. (2022). Concepts and consequences of a core gut microbiota for animal growth and development. Annual Review of Animal Biosciences, 10: 177-201. DOI:10.1146/annurev-animal-013020-020412

Phillipps, Q., & Phillipps, K. (2018). Phillipps field guide to the mammals of Borneo. 2nd Edition. Oxford, UK: John Beaufoy Publishing.

Risely, A. (2020). Applying the core microbiome to understand host–microbe systems. Journal of Animal Ecology, 89(7): 1549-1558. DOI:10.1111/1365-2656.13229

Sariyati, N.H., Othman, N., Abdullah‐Fauzi, N.A.F., Chan, E., Md‐Zain, B.M., Karuppannan, K.V., & Abdul‐Latiff, M.A.B. (2024). Characterizing the gastrointestinal microbiome diversity in endangered Malayan Siamang (Symphalangus syndactylus): Insights into group composition, age variability and sex‐related patterns. Journal of Medical Primatology, 53(5), e12730. DOI:10.1111/jmp.12730

Sharon, I., Quijada, N.M., Pasolli, E., Fabbrini, M., Vitali, F., Agamennone, V., Dötsch, A., Selberherr, E., Grau, J.H., Meixner, M., Liere, K., Ercolini, D., de Filippo, C., Caderni, G., Brigidi, P., & Turroni, S. (2022). The core human microbiome: Does it exist and how can we find It? A critical review of the concept. Nutrients, 14(14): 2872. DOI:10.3390/nu14142872

Taudière, A. (2023). MiscMetabar: Miscellaneous functions for metabarcoding analysis. Retrieved January 16, 2024, from https://github.com/adrientaudiere/MiscMetabar.

Teng, Y., Yang, X., Li, G., Zhu, Y., Zhang, Z. (2022). Habitats show more impacts than host species in shaping gut microbiota of sympatric rodent species in a fragmented forest. Frontiers in Microbiology, 13: 811990. DOI:10.3389/fmicb.2022.811990

Turnbaugh, P.J., Ley, R.E., Hamady, M., Fraser-Liggett, C.M., Knight, R., & Gordon, J.I. (2007). The human microbiome project. Nature, 449(7164): 804-810. DOI:10.1038/nature06244

Valdes, A.M., Walter, J., Segal, E., & Spector, T.D. (2018). Role of the gut microbiota in nutrition and health. BMJ, 361: k2179. DOI:10.1136/bmj.k2179

Viney, M. (2019). The gut microbiota of wild rodents: Challenges and opportunities. Laboratory Animals, 53(3): 252-258. DOI:10.1177/0023677218787538

Wang, J., Lang, T., Shen, J., Dai, J., Tian, L., & Wang, X. (2019). Core gut bacteria analysis of healthy mice. Frontiers in Microbiology, 10: 887. DOI:10.1128/AEM.00794-10

Wang, Z., Zhang, C., Li, G., & Yi, X. (2022). The influence of species identity and geographic locations on gut microbiota of small rodents. Frontiers in Microbiology, 13: 983660. DOI:10.3389/fmicb.2022.983660

Weldon, L., Abolins, S., Lenzi, L., Bourne, C., Riley, E.M., & Viney, M. (2015). The gut microbiota of wild mice. PLoS ONE, 10(8): e0134643. DOI: 10.1371/journal.pone.0134643

Wexler, H. M. (2007). Bacteroides: The good, the bad, and the nitty-gritty. Clinical Microbiology Reviews, 20(4), 593-621. DOI:10.1128/cmr.00008-07

Wickham, H. (2011). ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics, 3(2): 180-185. DOI:10.1002/wics.147

Wortelboer, K., Koopen, A.M., Herrema, H., de Vos, W.M., Nieuwdorp, M., & Kemper, E.M. (2022). From fecal microbiota transplantation toward next-generation beneficial microbes: The case of Anaerobutyricum soehngenii. Frontiers in Medicine, 9: 1077275. DOI:10.3389/fmed.2022.

Zheng, J., Wittouck, S., Salvetti, E., Franz, C.M., Harris, H.M., Mattarelli, P., O’Toole, P.W., Pot, B., Vandamme, P., Walter, J., Watanabe, K., Wuyts, S., Felis, G.E., Gänzle, M.G., & Lebeer, S. (2020). A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. International Journal of Systematic and Evolutionary Microbiology, 70(4): 2782-2858. DOI:10.1099/ijsem.0.004107

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Published

2024-12-23

How to Cite

AZMI, M. A. I., WILLIAM-DEE, J., MORNI, M. A., AZHAR, N. A. A., SABARUDIN, N. A.-S., JINGGONG, E. R., ZOLKAPLEY, S., TAN, C.-S., & ANWARALI KHAN, F. A. (2024). The Gut Microbiomes of Wild Rodents within Forested Environments in Sarawak, Borneo: Rodent Gut Microbiomes in Sarawak Forests. Borneo Journal of Resource Science and Technology, 14(2), 188–200. https://doi.org/10.33736/bjrst.7517.2024