The Melipona gut microbiota differs from other social bees, being characterized by the absence of crucial corbiculate core gut symbionts and a high occurrence of environmental strains. We studied the microbial diversity and composition of three Melipona species and their honey to understand which strains are obtained by horizontal transmission (HT) from the pollination environment, represent symbionts with HT from the hive/food stores or social transmission (ST) between nestmates. Bees harbored higher microbial alpha diversity and a different and more species-specific bacterial composition than honey. The fungal communities of bee and honey samples are also different but less dissimilar. As expected, the eusocial corbiculate core symbionts Snodgrassella and Gilliamella were absent in bees that had a prevalence of Lactobacillaceae - including Lactobacillus (formerly known as Firm-5), Bifidobacteriaceae, Acetobacteraceae, and Streptococcaceae - mainly strains close to Floricoccus, a putative novel symbiont acquired from flowers. They might have co-evolved with these bees via ST, and along with environmental Lactobacillaceae and Pectinatus (Veillonellaceae) strains obtained by HT, and Metschnikowia and Saccharomycetales yeasts acquired by HT from honey or the pollination environment, including plants/flowers, possibly compose the Melipona core microbiota. This work contributes to the understanding of Melipona symbionts and their modes of transmission.