This study describes the physiological properties of the widespread and recently described acid-tolerant microorganism Metallibacterium scheffleri DKE6. Despite that casitone was reported to be the only growth substrate of the organism, using a combination of proteomic, genomic and transcriptomic approaches as well as microbiological assays, we could identify a rather versatile metabolism. The detected casein hydrolysis was corroborated by the detection of proteases in the supernatant of the organism as well as in transcriptome studies. Genomic analysis identified amino acid auxotrophies, which were revealed as the reason for the observed growth deficiency with other substrates in the absence of casein. It was verified that glucose could serve as a growth substrate in the presence of amino acids as building blocks, a finding that was supported by the detection of three glycolytic pathways. Additionally, genes for sulfur and hydrogen oxidation were found, and sulfate formation could be shown during growth with tetrathionate. Metallibacterium scheffleri is able to raise the pH in acidic environments via ammonium production. Overall, the distribution of related Metallibacterium species demonstrates an adaption of this genus to diverse environments with varying pH values. Growth in biofilms or sediments also seems to be a common trait. We hypothesize that this biofilm growth supports the ability of Metallibacterium species to adapt to different pH values via formation of pH microniches.