Previous physiological studies of the genus Ferroplasma have indicated that these microorganisms are capable of fixing CO2 in the presence of ferrous iron and low concentrations of yeast extract. Analysis of the gene complement of Ferroplasma acidarmanus fer1 and two partial genomes of Ferroplasma type I and II derived from the Iron Mountain acid mine drainage metagenome revealed the absence of several functional marker genes encoding key enzymes of three know alternative CO2 fixation routes present in archaea, i.e. the 3-hydroxypropionate cycle, the Ljungdahl–Wood pathway and the reverse TCA cycle. It is thus intriguing how these chemoautotrophic archaeal species deal with their requirements for carbon and suggests that they might have a distinct CO2 fixation route, as yet unreported. Using comparative genomics and metabolic reconstruction strategies, a putative pathway was detected for C1 fixation consisting of four main steps: 1) conversion of carbon monoxide to carbon dioxide with gain of energy and/or 2) reduction of carbon dioxide to formate, 3) incorporation of formate to tetrahydrofolate and 4) donation of the carbon moiety of tetrahydrofolate to glycine to produce serine. Steps 1 to 3 involve enzymes that correspond to some of the Ljungdahl–Wood pathway proteins, whereas step 4 resembles the well known “serine cycle”, utilized by methylotrophic microorganisms for formaldehyde fixation. Thus, this chimaeric pathway might represent the missing carbon fixation route in Ferroplasmatales. Herein, we discuss the implications of these findings in the context of central carbon metabolism requirements for biomass production in acidic environments.