The present study describes for the first time the community composition and functional potential of the microbial mats found in the supratidal, gypsum-rich and hypersaline region of Blue Holes, Shark Bay. This was achieved via high-throughput metagenomic sequencing of total mat community DNA and complementary analyses using hyperspectral confocal microscopy. Mat communities were dominated by Proteobacteria (29%), followed by Bacteroidetes/Chlorobi group (11%) and Planctomycetes (10%). These mats were found to also harbour a diverse community of potentially novel microorganisms, including members from the DPANN, Asgard archaea and candidate phyla radiation, with highest diversity found in the lower regions (∼14-20 mm depth) of the mat. In addition to pathways for major metabolic cycles, a range of putative rhodopsins with previously uncharacterized motifs and functions were identified along with heliorhodopsins and putative schizorhodopsins. Critical microbial interactions were also inferred, and from 117 medium- to high-quality metagenome-assembled genomes, viral defence mechanisms (CRISPR, BREX and DISARM), elemental transport, osmoprotection, heavy metal resistance and UV resistance were also detected. These analyses have provided a greater understanding of these distinct mat systems in Shark Bay, including key insights into adaptive responses and proposing that photoheterotrophy may be an important lifestyle in Blue Holes.