Distinctive Microbiome Type Distribution in a Young Adult Balinese Cohort May Reflect Environmental Changes Associated with Modernization

Abstract

An important public health question is understanding how changes in human environments can drive changes in the gut microbiota that influence risks associated with human health and wellbeing. It is well-documented that the modernization of societies is strongly correlated with intergenerational change in the frequency of nutrition-related chronic diseases in which microbial dysbiosis is implicated. The population of Bali, Indonesia, is well-positioned to study the interconnection between a changing food environment and microbiome patterns in its early stages, because of a recent history of modernization. Here, we characterize the fecal microbiota and diet history of the young adult women in Bali, Indonesia (n = 41) in order to compare microbial patterns in this generation with those of other populations with different histories of a modern food environment (industrialized supply chain). We found strong support for two distinct fecal microbiota community types in our study cohort at similar frequency: a Prevotella-rich (Type-P) and a Bacteroides-rich (Type-B) community (p < 0.001, analysis of similarity, Wilcoxon test). Although Type-P individuals had lower alpha diversity (p < 0.001, Shannon) and higher incidence of obesity, multivariate analyses with diet data showed that community types significantly influenced associations with BMI. In a multi-country dataset (n = 257), we confirmed that microbial beta diversity across subsistent and industrial populations was significantly associated with Prevotella and Bacteroides abundance (p < 0.001, generalized additive model) and that the prevalence of community types differs between societies. The young adult Balinese microbiota was distinctive in having an equal prevalence of two community types. Collectively, our study showed that the incorporation of community types as an explanatory factor into study design or modeling improved the ability to identify microbiome associations with diet and health metrics.

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Data availability

The Balinese dataset supporting the conclusions of this article is available in the European Nucleotide Archive repository, project code PRJEB32385. Datasets for other populations are available in the MG-RAST repository, project numbers mgp401 and mgp7058.

Code Availability

Complete accounts of statistical analyses and R scripts are provided in the Online Resource 1 of this publication.

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Acknowledgements

We are grateful to university students at the Faculty of Medicine, Udayana University, Denpasar (Tjokorda Istri Pramitasuri and colleagues), who had assisted the study during the recruitment, enrolment, and data collection stage in Denpasar. We thank Prodia Laboratory in Denpasar for supporting the collection and initial storage of the samples. We are grateful to Prof. Sangkot Marzuki at Indonesia Science Academy (Akademi Ilmu Pengetahuan Indonesia) for facilitating and supporting the commencement of this study. We thank our colleagues, Sukma Oktavianthi, Lidwina Priliani, Hidayat Trimarsanto, Eline Klaassens, and Mark Read for their input and guidance.

Funding

This research was partially supported by the Indonesia Ministry of Research and Technology/National Agency for Research and Innovation through the Eijkman Institute for Molecular Biology; Australia’s Department of Foreign Affairs and Trade through the Australia Awards Scholarship; and the International Program Development Fund (2013 Round).

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Authors

Contributions

CAF, SGM, AJH, IWW, DMW, and HS performed sampling. CAF proposed the study, did laboratory work, analyzed the data, and drafted the manuscript. SGM, HS, and AJH designed, directed, and facilitated the study and provided major support in the data interpretation. DMW and IWW coordinated and facilitated the study enrolment, including the collection and interpretation of diet and demographic data. RD and RM provided support for the analysis and interpretation of diet data.

Corresponding author

Correspondence to Andrew J. Holmes.

Ethics declarations

Ethics Approval

The ethical permit for this study was granted by the Udayana University Faculty of Medicine and Sanglah Hospital Ethics Commission on 18 September 2014 in Denpasar, Indonesia (No. 1286/UN.14.2/Litbang/2014). The permit was endorsed by the Eijkman Institute Research Ethics Commission on 24 December 2014 in Jakarta, Indonesia (Permit No. 80).

Consent to Participate

Written consent for participation in this study was obtained from all study participants.

Consent for Publication

Written consent for publication of data was obtained from all study participants. All data has been de-identified to protect the privacy of the study participants.

Competing Interests

The authors declare no competing interests.

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Cite this article

Febinia, C.A., Malik, S.G., Djuwita, R. et al. Distinctive Microbiome Type Distribution in a Young Adult Balinese Cohort May Reflect Environmental Changes Associated with Modernization. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01786-9

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Keywords

  • Microbiome
  • Fecal
  • Community assembly
  • Bali
  • Lifestyle
  • Population
  • Heterogeneity