Microbial coexistence in complex communities requires mechanisms that minimize competition and optimize resource use. Here, we show that bacteria modulate protein abundance in response to specific community members, reducing functional redundancy and promoting metabolic complementarity. Using synthetic gut-derived consortia exposed to distinct carbon sources, we systematically profiled proteomic responses of individual species across isolate, pairwise, and four-member communities. We found that biotic interactions, rather than abiotic conditions, were the dominant drivers of proteomic variation. These interactions led to reproducible, partner-specific expression shifts that significantly reduced functional overlap and were frequently associated with increased community productivity. Our findings reveal that microbes dynamically reshape their realized niche through protein abundance plasticity, enabling them to partition metabolic space and stabilize community structure. This study provides a mechanistic link between microbial interaction networks, regulatory flexibility, and coexistence, offering a generalizable framework for understanding and engineering functional microbial ecosystems.