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Abstract Whole microbial communities regularly merge with one another, often in tandem with their environments, in a process called community coalescence. Such events impose substantial changes: abiotic perturbation from environmental blending and biotic perturbation of community merging. We used an aquatic mixing experiment to unravel the effects of these perturbations on the whole microbiome response and on the success of individual taxa when distinct freshwater and marine communities coalesce. We found that an equal mix of freshwater and marine habitats and blended microbiomes resulted in strong convergence of the community structure toward that of the marine microbiome. The enzymatic potential of these blended microbiomes in mixed media also converged toward that of the marine, with strong correlations between the multivariate response patterns of the enzymes and of community structure. Exposing each endmember inocula to an axenic equal mix of their freshwater and marine source waters led to a 96% loss of taxa from our freshwater microbiomes and a 66% loss from our marine microbiomes. When both inocula were added together to this mixed environment, interactions amongst the communities led to a further loss of 29% and 49% of freshwater and marine taxa, respectively. Under both the axenic and competitive scenarios, the diversity lost was somewhat counterbalanced by increased abundance of microbial taxa that were too rare to detect in the initial inocula. Our study emphasizes the importance of the rare biosphere as a critical component of microbial community responses to community coalescence.