The waxy mutation in sorghum and other cereal grains reshapes the gut microbiome by reducing levels of multiple beneficial species

ABSTRACT

Waxy starches from cereal grains contain >90% amylopectin due to naturally occurring mutations that block amylose biosynthesis. Waxy starches have unique organoleptic characteristics (e.g. sticky rice) as well as desirable physicochemical properties for food processing. Using isogenic pairs of wild type sorghum lines and their waxy derivatives, we studied the effects of waxy starches in the whole grain context on the human gut microbiome. In vitro fermentations with human stool microbiomes show that beneficial taxonomic and metabolic signatures driven by grain from wild type parental lines are lost in fermentations of grain from the waxy derivatives and the beneficial signatures can be restored by addition of resistant starch. These undesirable effects are conserved in fermentations of waxy maize, wheat, rice and millet. We also demonstrate that humanized gnotobiotic mice fed low fiber diets supplemented with 20% grain from isogenic pairs of waxy vs. wild type parental sorghum have significant differences in microbiome composition and show increased weight gain. We conclude that the benefits of waxy starches on food functionality can have unintended tradeoff effects on the gut microbiome and host physiology that could be particularly relevant in human populations consuming large amounts of waxy grains.

KEYWORDS:

• Waxy starch
• resistant starch
• sorghum
• gut microbiome
• butyrate
• Roseburia
• Christensenellaceae

Availability of data and materials

The sequence data reported in this paper have been deposited in the NCBI database (PRJNA811321).

Ethical approval and consent to participate

All procedures involving human subjects were approved by the Institutional Review Board of the University of Nebraska–Lincoln before initiating the study (20160816311EP). Informed consent was obtained from all subjects prior to fecal collection. The Institutional Animal Care and Use Committee at the University of Nebraska-Lincoln approved all procedures involving animals (protocol 1700).

Acknowledgments

This work was completed utilizing the Holland Computing Center of the University of Nebraska which receives support from the Nebraska Research Initiative. We thank the technical staff from the Nebraska Gnotobiotic Mouse Program for outstanding animal husbandry.

Authors’ contributions

QY: conceptualization, methodology, formal analysis, investigation, writing - original draft, writing - review & editing. MVH: methodology, investigation, review & editing. NK: methodology. SS: resources, methodology, writing - review & editing. DR: conceptualization, methodology, resources, review & editing. AJ: methodology, investigation, review & editing. JS: methodology, investigation. KB: methodology, investigation. JP: methodology, investigation. JT: resources, methodology, investigation, review & editing. ART: conceptualization, methodology, resources, review & editing. AB: conceptualization, resources, writing - original draft, writing - review & editing, supervision, funding acquisition.

Disclosure statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2178799

Additional information

Funding

This research was supported by funds from the Jeff and Tricia Raikes Foundation, the Bill and Melinda Gates Foundation, the Don Dillon Foundation to A.K.B., and USDA-ARS project 3042-21220-033-00D. Q.Y. was supported in part by scholarship from the China Scholarship Council and N.K. was supported in part by Foundation for Food and Agriculture Research (FFAR) and the FFAR Fellows Program;