Interplay between particle size and microbial ecology in the gut microbiome

Jeffrey Letourneau, Verónica M Carrion, Jun Zeng, Sharon Jiang, Olivia W Osborne, Zachary C Holmes, Aiden Fox, Piper Epstein, Chin Yee Tan, Michelle Kirtley, Neeraj K Surana, Lawrence A David
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Abstract

Physical particles can serve as critical abiotic factors that structure the ecology of microbial communities. For non-human vertebrate gut microbiomes, fecal particle size (FPS) has been known to be shaped by chewing efficiency and diet. However, little is known about what drives FPS in the human gut. Here, we analyzed FPS by laser diffraction across a total of 76 individuals and found FPS to be strongly individualized. Contrary to our initial hypothesis, a behavioral intervention with 41 volunteers designed to increase chewing efficiency did not impact FPS. Dietary patterns could also not be associated with FPS. Instead, we found evidence that human and mouse gut microbiomes shaped FPS. Fecal samples from germ-free and antibiotic-treated mice exhibited increased FPS relative to colonized mice. In humans, markers of longer transit time were correlated with smaller FPS. Gut microbiota diversity and composition were also associated with FPS. Finally, ex vivo culture experiments using human fecal microbiota from distinct donors showed that differences in microbiota community composition can drive variation in particle size. Together, our results support an ecological model in which the human gut microbiome plays a key role in reducing the size of food particles during digestion. This finding has important implications for our understanding of energy extraction and subsequent uptake in gastrointestinal tract. FPS may therefore be viewed as an informative functional readout, providing new insights into the metabolic state of the gut microbiome.
肠道微生物群中颗粒大小与微生物生态之间的相互作用
物理颗粒可以作为构建微生物群落生态的关键非生物因素。对于非人类脊椎动物的肠道微生物群落来说,粪便颗粒大小(FPS)是由咀嚼效率和饮食决定的。然而,人们对人类肠道中粪便颗粒大小的驱动因素知之甚少。在这里,我们通过激光衍射分析了总共 76 个个体的粪便颗粒大小,发现粪便颗粒大小具有很强的个体差异性。与我们最初的假设相反,对 41 名志愿者进行的旨在提高咀嚼效率的行为干预并没有影响 FPS。饮食模式也与 FPS 无关。相反,我们发现了人类和小鼠肠道微生物群影响 FPS 的证据。无菌小鼠和经过抗生素处理的小鼠的粪便样本显示,与定植小鼠相比,FPS 增加了。在人类中,转运时间较长的标志物与较小的FPS相关。肠道微生物群的多样性和组成也与 FPS 相关。最后,使用来自不同供体的人类粪便微生物群进行的体外培养实验表明,微生物群落组成的差异可导致颗粒大小的变化。总之,我们的研究结果支持一种生态学模型,在该模型中,人类肠道微生物群在消化过程中缩小食物颗粒大小方面发挥着关键作用。这一发现对我们理解胃肠道的能量提取和后续吸收具有重要意义。因此,FPS 可被视为一种信息丰富的功能读数,为了解肠道微生物组的新陈代谢状态提供了新的视角。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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