A Cross-Scale Neutral Theory Approach to the Influence of Obesity on Community Assembly of Human Gut Microbiome

Abstract

Background: The implications of gut microbiome to obesity have been extensively investigated in recent years although the exact mechanism is still unclear. The question whether or not obesity influences gut microbiome assembly has not been addressed. The question is significant because it is fundamental for investigating the diversity maintenance and stability of gut microbiome, and the latter should hold a key for understanding the etiological implications of gut microbiome to obesity. Methods: In this study, we adopt a dual neutral theory modeling strategy to address this question from both species and community perspectives, with both discrete and continuous neutral theory models. The first neutral theory model we apply is Hubbell's neutral theory of biodiversity that has been extensively tested in macro-ecology of plants and animals, and the second we apply is Sloan's neutral theory model that was developed particularly for microbial communities based on metagenomic sequencing data. Both the neutral models are complementary to each other and integrated together offering a comprehensive approach to more accurately revealing the possible influence of obesity on gut microbiome assembly. This is not only because the focus of both neutral theory models is different (community vs. species), but also because they adopted two different modeling strategies (discrete vs. continuous). Results: We test both the neutral theory models with datasets from Turnbaugh et al. (2009). Our tests showed that the species abundance distributions of more than ½ species (59-69%) in gut microbiome satisfied the prediction of Sloan's neutral theory, although at the community level, the number of communities satisfied the Hubbell's neutral theory was negligible (2 out of 278). Conclusion: The apparently contradictory findings above suggest that both stochastic neutral effects and deterministic environmental (host) factors play important roles in shaping the assembly and diversity of gut microbiome. Furthermore, obesity may just be one of the host factors, but its influence may not be strong enough to tip the balance between stochastic and deterministic forces that shape the community assembly. Finally, the apparent contradiction from both the neutral theories should not be surprising given that there are still near 30-40% species that do not obey the neutral law.

Keywords: Hubbell neutral theory of biodiversity; Sloan's neutral model for microbes; community assembly; niche theory; obesity; species abundance distribution (SAD).

Figure 1

The rank abundance curves of two community samples that successfully passed the neutrality test: the solid red line represents for the observed community and the black dash lines for the simulated communities based on the neutral theory model. The X-axis is the species rank order in abundance and Y-axis is the abundance of each species in natural logarithm.

Figure 2

The percentages of the neutral (green) and non-neutral (red) species, respectively, in the three regimes designed for testing Sloan's neutral theory.