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Auxotrophs are prevalent in microbial communities, enhancing their diversity and stability-a counterintuitive effect considering their dependence on essential resources from other species. To address the ecological roles of auxotrophs, our study introduced a consumer-resource model (CRM) to capture the complex higher-order interactions within these communities. We also developed an intuitive graphical and algebraic framework, which assesses the feasibility of auxotroph communities and their stability under resource fluctuations and biological invasions. Validated against experimental data from synthetic E. coli auxotroph communities, the model accurately predicted outcomes of community assembly. Our findings highlight the critical role of higher-order interactions and resource dependencies in maintaining the diversity and stability of microbial ecosystems dominated by auxotrophs. A record of this paper's transparent peer review process is included in the supplemental information.