Chemosynthesis enhances carbon fixation in an active microbialite ecosystem

Microbialites—carbonate structures formed under the influence of microbial action— are the earliest macroscopic evidence of life. For three billion years, the microbial mat communities responsible for these structures fundamentally shaped Earth’s biogeochemical cycles. In photosynthetic microbial communities, light energy ultimately drives primary production and the ensuing cascade of daisy-chained metabolisms. However, reduced compounds such as atmospheric trace gases and those released as metabolic byproducts in deeper, anaerobic regions of the mat, could also fuel chemosynthetic processes. Here, we investigated the intricate metabolic synergies that sustain microbialite community nutrient webs. We recovered 331 genomes spanning 40 bacterial and archaeal phyla, revealing a staggering diversity fuelled by the biogeochemistry of these ecosystems. While phototrophy is an important metabolism encoded by 17% of the genomes, over half encode enzymes to harness energy from reduced compounds and 12% co-encode carbon fixation pathways, using sulfide and hydrogen as major electron donors. Consistent with these genomic predictions, we experimentally demonstrated that microbialite communities oxidise ferrous iron, ammonia, sulfide and gas substrates aerobically and anaerobically. Furthermore, ¹⁴ C-fixation assays revealed that chemosynthesis contributes significantly to carbon fixation alongside photosynthesis. Chemosynthesis in microbialite communities represents a complex interplay of metabolic synergies and continuous nutrient cycling, which decouples community carbon fixation from the diurnal cycle. As a result, this process mitigates the loss of organic carbon from respiration, thus enhancing the net productivity of these highly efficient ecosystems.