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

Authors: YANG, QINNAN - University Of Nebraska; VAH HAUTE, MALLORY - University Of Nebraska; KORTH, NATE - University Of Nebraska; Sattler, Scott; ROSE, DEVIN - University Of Nebraska; PRICE, JEFF - University Of Nebraska; BEEDE, KRISTIN - University Of Nebraska; RAMER-TAIT, AMANDA - University Of Nebraska; Toy, John

Submitted to: Gut Microbes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2023
Publication Date: 2/21/2023
Citation: Yang, Q., Vah Haute, M., Korth, N., Sattler, S.E., Rose, D., Price, J., Beede, K., Ramer-Tait, A.E., Toy, J.J. 2023. The waxy mutation in sorghum and other cereal grains reshapes the gut microbiome by reducing levels of multiple beneficial species. Gut Microbes. 15(1):2178799. https://doi.org/10.1080/19490976.2023.2178799.
DOI: https://doi.org/10.1080/19490976.2023.2178799

Interpretive Summary: Starch is an important food ingredient, which is often modified to chemically change its properties in food products. Grains containing mutations in the Granule Bound Starch Synthase gene, also referred to as ‘waxy’, have altered starch composition. This altered starch composition affects the physical properties of the starch and increases its digestibility. Grain from normal and waxy sorghum was examined for its effects on human colon microbiome using in vitro experiments. The normal sorghum starch is more resistant to digestion, which led to increased levels of bacteria beneficial to human health compared to waxy grain. Adding starch from normal sorghum to the waxy grain restored the growth of these beneficial bacteria in the experiments. Similar effects of waxy starches from maize, wheat, rice, and millet on these bacteria were also observed. Germ-free mice were given human microbiomes used in the experiments and fed diets with whole grain from normal or waxy sorghum. Significant differences in bacterial composition were found across all mice that consumed the waxy sorghum diet compared to the normal one. In addition, the mice consuming waxy sorghum grain also gained more weight. The conclusion was waxy starch has potentially undesirable effects on the human microbiome. Examining effects of plant traits on the human microbiome opens new avenues to improve plants for human health.

Technical 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.