Gut microbiota-driven metabolic alterations reveal gut-brain communication in Alzheimer's disease model mice

Gut Microbes. 2024 Jan-Dec;16(1):2302310. doi: 10.1080/19490976.2024.2302310. Epub 2024 Jan 23.

Abstract

The gut microbiota (GM) and its metabolites affect the host nervous system and are involved in the pathogeneses of various neurological diseases. However, the specific GM alterations under pathogenetic pressure and their contributions to the "microbiota - metabolite - brain axis" in Alzheimer's disease (AD) remain unclear. Here, we investigated the GM and the fecal, serum, cortical metabolomes in APP/PS1 and wild-type (WT) mice, revealing distinct hub bacteria in AD mice within scale-free GM networks shared by both groups. Moreover, we identified diverse peripheral - central metabolic landscapes between AD and WT mice that featured bile acids (e.g. deoxycholic and isodeoxycholic acid) and unsaturated fatty acids (e.g. 11Z-eicosenoic and palmitoleic acid). Machine-learning models revealed the relationships between the differential/hub bacteria and these metabolic signatures from the periphery to the brain. Notably, AD-enriched Dubosiella affected AD occurrence via cortical palmitoleic acid and vice versa. Considering the transgenic background of the AD mice, we propose that Dubosiella enrichment impedes AD progression via the synthesis of palmitoleic acid, which has protective properties against inflammation and metabolic disorders. We identified another association involving fecal deoxycholic acid-mediated interactions between the AD hub bacteria Erysipelatoclostridium and AD occurrence, which was corroborated by the correlation between deoxycholate levels and cognitive scores in humans. Overall, this study elucidated the GM network alterations, contributions of the GM to peripheral - central metabolic landscapes, and mediatory roles of metabolites between the GM and AD occurrence, thus revealing the critical roles of bacteria in AD pathogenesis and gut - brain communications under pathogenetic pressure.

Keywords: Alzheimer’s disease; bacterial co-occurrence network; gut microbiota; gut–brain communication; mediation effect; metabolomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease*
  • Animals
  • Brain
  • Communication
  • Firmicutes
  • Gastrointestinal Microbiome*
  • Humans
  • Mice
  • Microbiota*

Grants and funding

This study was supported in part by the National Key R&D Program of China (2021YFE0203000), the National Natural Science Foundation of China (NSFC)/RGC Joint Research Scheme (32061160472), the Guangdong Provincial Fund for Basic and Applied Basic Research (2019B1515130004 and 2019A1515011425), the Guangdong Provincial Key S&T Program (2018B030336001), the Shenzhen Knowledge Innovation Program (JCYJ20220818100800001, JCYJ20200109115631248, and ZDSYS20200828154800001), and the Fundamental research program of Shenzhen Virtual University Park (2021Szvup137).