Comparative analysis of gut microbiota between common (Macaca fascicularis fascicularis) and Burmese (M. f. aurea) long-tailed macaques in different habitats.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 09 2023
11 09 2023
Historique:
received:
17
05
2023
accepted:
06
09
2023
medline:
13
9
2023
pubmed:
12
9
2023
entrez:
11
9
2023
Statut:
epublish
Résumé
The environment has an important effect on the gut microbiota-an essential part of the host's health-and is strongly influenced by the dietary pattern of the host as these together shape the composition and functionality of the gut microbiota in humans and other animals. This study compared the gut microbiota of Macaca fascicularis fascicularis and M. f. aurea in mangrove and island populations using 16S rRNA gene sequencing on a nanopore platform to investigate the effect of the environment and/or diet. The results revealed that the M. f. fascicularis populations that received anthropogenic food exhibited a higher richness and evenness of gut microbiota than the M. f. aurea populations in different habitats. Firmicutes and Bacteroidetes were the two most abundant bacterial phyla in the gut microbiota of both these subspecies; however, the relative abundance of these phyla was significantly higher in M. f. aurea than in M. f. fascicularis. This variation in the gut microbiota between the two subspecies in different habitats mostly resulted from the differences in their diets. Moreover, the specific adaptation of M. f. aurea to different environments with a different food availability had a significant effect on their microbial composition.
Identifiants
pubmed: 37696929
doi: 10.1038/s41598-023-42220-z
pii: 10.1038/s41598-023-42220-z
pmc: PMC10495367
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14950Informations de copyright
© 2023. Springer Nature Limited.
Références
Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).
pubmed: 16741115
pmcid: 3027896
Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 95, 6578–6583 (1998).
pubmed: 9618454
pmcid: 33863
Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).
pubmed: 20203603
pmcid: 3779803
Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012).
pubmed: 22968153
Grenham, S., Clarke, G., Cryan, J. F. & Dinan, T. G. Brain-gut-microbe communication in health and disease. Front. Physiol. 2, 1–15 (2011).
Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L. & Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011).
pubmed: 21677749
pmcid: 3298082
Watanabe, K. et al. Microbiome-mediated neutrophil recruitment via CXCR2 and protection from amebic colitis. PLoS Pathog. 13, 1–20 (2017).
Zhu, B., Wang, X. & Li, L. Human gut microbiome: The second genome of human body. Protein Cell 1, 718–725 (2010).
pubmed: 21203913
pmcid: 4875195
Ferreira, C. M. et al. The central role of the gut microbiota in chronic inflammatory diseases. J. Immunol. Res. 2014, 1–12 (2014).
Kennedy, P. J., Cryan, J. F., Dinan, T. G. & Clarke, G. Irritable bowel syndrome: A microbiome-gut-brain axis disorder?. World J. Gastroenterol. 20, 14105–14125 (2014).
pubmed: 25339800
pmcid: 4202342
Baothman, O. A., Zamzami, M. A., Taher, I., Abubaker, J. & Abu-Farha, M. The role of gut microbiota in the development of obesity and diabetes. Lipids Health Dis. 15, 1–8 (2016).
Bisgaard, H. et al. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Aller. Clin. Immunol. 128, 646–652 (2011).
Goodrich, J. K. et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731–743 (2016).
pubmed: 27173935
pmcid: 4915943
Hale, V. L. et al. Diet versus phylogeny: A comparison of gut microbiota in captive colobine monkey species. Microb. Ecol. 75, 515–527 (2018).
pubmed: 28735426
Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).
pubmed: 29995839
De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107, 14691–14696 (2010).
pubmed: 20679230
pmcid: 2930426
Lin, A. et al. Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS ONE 8, 1–19 (2013).
Sun, B. et al. Marked variation between winter and spring gut microbiota in free-ranging Tibetan macaques (Macaca thibetana). Sci. Rep. 6, 1–8 (2016).
Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).
pubmed: 25524570
Zhao, J. et al. Characterization of the gut microbiota in six geographical populations of Chinese rhesus macaques (Macaca mulatta), implying an adaptation to high-altitude environment. Microb. Ecol. 76, 565–577 (2018).
pubmed: 29372281
Claesson, M. J. et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178–184 (2012).
pubmed: 22797518
Lan, D. et al. Correlations between gut microbiota community structures of Tibetans and geography. Sci. Rep. 7, 1–9 (2017).
Fooden, J. Systematic review of Southeast Asian longtail macaques, Macaca fascicularis (Raffles, [1821]). Fieldiana Zool. 81, 1–206 (1995).
Malaivijitnond, S. et al. Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). Am. J. Primatol. 69, 227–233 (2007).
pubmed: 17146796
Malaivijitnond, S., Vazquez, Y. & Hamada, Y. Human impact on long-tailed macaques in Thailand in Monkeys on the Edge: Ecology and Management of Long-Tailed Macaques and their Interface with Humans (eds. Gumert, M. D. & Jones-Engel, L.) 118–158 (Cambridge University Press, UK, 2011).
Bandini, E. & Tennie, C. Naive, captive long-tailed macaques (Macaca fascicularis fascicularis) fail to individually and socially learn pound-hammering, a tool-use behaviour. R. Soc. Open Sci. 5, 1–17 (2018).
Bunlungsup, S. et al. Morphological characteristics and genetic diversity of Burmese long-tailed Macaques (Macaca fascicularis aurea). Am. J. Primatol. 78, 441–455 (2016).
pubmed: 26670099
Osada, N., Matsudaira, K., Hamada, Y. & Malaivijitnond, S. Testing sex-biased admixture origin of macaque species using autosomal and X-chromosomal genomic sequences. Genome Biol. Evol. 13, 1–14 (2021).
Matsudaira, K. et al. Whole mitochondrial genomic and Y-chromosomal phylogenies of Burmese long-tailed macaque (Macaca fascicularis aurea) suggest ancient hybridization between fascicularis and sinica species groups. J. Hered. 109, 360–371 (2018).
pubmed: 29186474
Phadphon, P., Kanthaswamy, S., Oldt, R. F., Hamada, Y. & Malaivijitnond, S. Population structure of Macaca fascicularis aurea, and their genetic relationships with M. f. fascicularis and M. mulatta determined by 868 RADseq-derived autosomal SNPs—A consideration for biomedical research. J. Med. Primatol. 51, 33–44 (2022).
pubmed: 34825374
Gumert, M. D. et al. Prevalence of tool behaviour is associated with pelage phenotype in intraspecific hybrid long-tailed macaques (Macaca fascicularis aurea × M. f fascicularis). Behaviour 156, 1083–1125 (2019).
Gumert, M. D., Kluck, M. & Malaivijitnond, S. The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman sea region of Thailand. Am. J. Primatol. 71, 594–608 (2009).
pubmed: 19405083
Luncz, L. V. et al. Group-specific archaeological signatures of stone tool use in wild macaques. Elife 8, 1–21 (2019).
Sawaswong, V. et al. High diversity and novel enteric viruses in fecal viromes of healthy wild and captive Thai cynomolgus macaques (Macaca fascicularis). Viruses 11, 1–19 (2019).
Sawaswong, V. et al. Oral-fecal mycobiome in wild and captive cynomolgus macaques (Macaca fascicularis). Fungal Genet. Biol. 144, 1–9 (2020).
Sawaswong, V. et al. Comparative analysis of oral-gut microbiota between captive and wild long-tailed macaque in Thailand. Sci. Rep. 11, 1–13 (2021).
Sawaswong, V. et al. Alteration of gut microbiota in wild-borne long-tailed macaques after 1-year being housed in hygienic captivity. Sci. Rep. 13, 5842 (2023).
pubmed: 37037869
pmcid: 10085984
Gumert, M. D. & Malaivijitnond, S. Marine prey processed with stone tools by Burmese long-tailed macaques (Macaca fascicularis aurea) in intertidal habitats. Am. J. Phys. Anthropol. 149, 447–457 (2012).
pubmed: 23042618
Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, 1–18 (2011).
Chen, T., Li, Y., Liang, J., Li, Y. & Huang, Z. Gut microbiota of provisioned and wild rhesus macaques (Macaca mulatta) living in a limestone forest in southwest Guangxi. China. Microbiologyopen 9, 1–15 (2020).
McKenzie, V. J. et al. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57, 690–704 (2017).
pubmed: 28985326
pmcid: 5978021
Nelson, T. M., Rogers, T. L., Carlini, A. R. & Brown, M. V. Diet and phylogeny shape the gut microbiota of Antarctic seals: A comparison of wild and captive animals. Environ. Microbiol. 15, 1132–1145 (2013).
pubmed: 23145888
Eckburg, P. B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635–1638 (2005).
pubmed: 15831718
pmcid: 1395357
Fogel, A. T. The gut microbiome of wild lemurs: A comparison of sympatric Lemur catta and Propithecus verreauxi. Folia Primatol. 86, 85–95 (2015).
Gomez, A. et al. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol. Ecol. 24, 2551–2565 (2015).
pubmed: 25846719
Trosvik, P., Rueness, E. K., De Muinck, E. J., Moges, A. & Mekonnen, A. Ecological plasticity in the gastrointestinal microbiomes of Ethiopian chlorocebus monkeys. Sci. Rep. 8, 1–20 (2018).
Kaakoush, N. O. Insights into the role of Erysipelotrichaceae in the human host. Front. Cell Infect. Microbiol. 5, 1–4 (2015).
Clarke, S. F. et al. Targeting the microbiota to address diet-induced obesity: A time dependent challenge. PLoS ONE 8, 1–9 (2013).
Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).
pubmed: 17183312
Fernando, S. C. et al. Rumen microbial population dynamics during adaptation to a high-grain diet. Appl. Environ. Microbiol. 76, 7482–7490 (2010).
pubmed: 20851965
pmcid: 2976194
Lapébie, P., Lombard, V., Drula, E., Terrapon, N. & Henrissat, B. Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat. Commun. 10, 1–7 (2019).
Chen, Z. et al. Diversity of macaque microbiota compared to the human counterparts. Sci. Rep. 8, 1–15 (2018).
Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 (2011).
pubmed: 21885731
pmcid: 3368382
Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1–18 (2018).
Iino, T., Mori, K., Tanaka, K., Suzuki, K. I. & Harayama, S. Oscillibacter valericigenes gen. nov., sp. Nov., a valerate-producing anaerobic bacterium isolated from the alimentary canal of a Japanese corbicula clam. Int. J. Syst. Evol. Microbiol. 57, 1840–1845 (2007).
pubmed: 17684268
Mondot, S. et al. Highlighting new phylogenetic specificities of Crohn’s disease microbiota. Inflamm. Bowel. Dis. 17, 185–192 (2011).
pubmed: 20722058
Sokol, H. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 105(43), 16731–16736 (2008).
pubmed: 18936492
pmcid: 2575488
Carlsson, A. H. et al. Faecalibacterium prausnitzii supernatant improves intestinal barrier function in mice DSS colitis. Scand. J. Gastroenterol. 48, 1136–1144 (2013).
pubmed: 23971882
Sokol, H. et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 15, 1183–1189 (2009).
pubmed: 19235886
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).
pubmed: 22972295
pmcid: 3577372
Wang, X., Maegawa, T., Karasawa, T., Ozaki, E. & Nakamura, S. Clostridium sardiniense Prévot 1938 and Clostridium absonum Nakamura et al. 1973 are heterotypic synonyms: Evidence from phylogenetic analyses of phospholipase C and 16S rRNA sequences, and DNA relatedness. Int. J. Syst. Evol. Microbiol. 55, 1193–1197 (2005).
pubmed: 15879254
Girinathan, B. P. et al. In vivo commensal control of Clostridioides difficile virulence. Cell Host Microbe 29, 1693–1708 (2021).
pubmed: 34637781
pmcid: 8651146
Tavella, T. et al. Elevated gut microbiome abundance of Christensenellaceae, Porphyromonadaceae and Rikenellaceae is associated with reduced visceral adipose tissue and healthier metabolic profile in Italian elderly. Gut Microbes 13, 1–19 (2021).
pubmed: 33557667
Watanabe, Y., Nagai, F. & Morotomi, M. Characterization of Phascolarctobacterium succinatutens sp. nov., an asaccharolytic, succinate-utilizing bacterium isolated from human feces. Appl. Environ. Microbiol. 78, 511–518 (2012).
pubmed: 22081579
pmcid: 3255759
Sharma, A. Virulence mechanisms of Tannerella forsythia. Periodontol 2000(54), 106–116 (2010).
Lourenço, T. G. B. et al. Microbial signature profiles of periodontally healthy and diseased patients. J. Clin. Periodontol. 41, 1027–1036 (2014).
pubmed: 25139407
pmcid: 4213353
Yoon, J. et al. Haloferula rosea gen. nov., sp. nov., Haloferulaharenae sp. nov., Haloferula phyci sp. Nov., Haloferula helveola sp. nov. and Haloferula sargassicola sp. nov., five marine representatives of the family Verrucomicrobiaceae within the phylum ‘Verrucomicrobia’. Int. J. Syst. Evol. Microbiol. 58, 2491–2500 (2008).
pubmed: 18984682
Peterson, J. et al. The NIH human microbiome project. Genome Res. 19, 2317–2323 (2009).
pubmed: 19819907
pmcid: 2792171
Yoon, S.-H. et al. Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613 (2017).
pubmed: 28005526
pmcid: 5563544
Watanabe, Y., Nagai, F., Morotomi, M., Sakon, H. & Tanaka, R. Bacteroides clarus sp. nov., Bacteroides fluxus sp. nov. and Bacteroides oleiciplenus sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 60, 1864–1869 (2010).
pubmed: 19767355
Cobo, F. et al. First case of abdominal infection caused by Bacteroides fluxus. Anaerobe 69, 102363 (2021).
pubmed: 33819627
Biddle, A., Stewart, L., Blanchard, J. & Leschine, S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5, 627–640 (2013).
Furet, J. P. et al. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol. Ecol. 68, 351–362 (2009).
pubmed: 19302550
Matsuo, Y. et al. Full-length 16S rRNA gene amplicon analysis of human gut microbiota using MinION™ nanopore sequencing confers species-level resolution. BMC Microbiol. 21, 1–13 (2021).
Wick, R. R., Judd, L. M. & Holt, K. E. Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biol. 20, 1–10 (2019).
Lanfear, R., Schalamun, M., Kainer, D., Wang, W. & Schwessinger, B. MinIONQC: Fast and simple quality control for MinION sequencing data. Bioinformatics 35, 523–525 (2019).
pubmed: 30052755
Wick, R., Porechop. [(accessed on 25 December 2022)]; Available online: https://github.com/rrwick/Porechop
Rodríguez-Pérez, H., Ciuffreda, L. & Flores, C. NanoCLUST: a species-level analysis of 16S rRNA nanopore sequencing data. Bioinformatics 37, 1600–1601 (2021).
pubmed: 33079990
Cole, J. R. et al. The ribosomal database project (RDP-II): Previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31, 442–443 (2003).
pubmed: 12520046
pmcid: 165486
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 850–852 (2019).
Chong, J., Liu, P., Zhou, G. & Xia, J. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat. Protoc. 15, 799–821 (2020).
pubmed: 31942082