Historic mine waste contains diverse microbial communities that reflect waste type and geochemistry.

Waste rock and tailings left behind by historic mining operations can contain substantial critical mineral resources. However, over the decades and centuries, since these deposits were emplaced, microbial communities developed that can catalyze rock weathering and elemental cycling, which could have impacted the economic resources but also might be harnessed for future biomining or other metal recovery efforts. Here, we combined microbial cell counting, rRNA gene and transcript sequencing, and whole rock geochemistry to compare the composition and abundance of microbial communities from five inactive mine sites in south-central New Mexico that contain critical minerals. While acidic seeps and adits at the sites contained organisms commonly found in acid rock drainage and bioleaching operations, these organisms were only present at very low abundance in the waste rock and tailings, which were instead dominated by bacteria and archaea that are related to inorganic nitrogen- and organic carbon-oxidizing taxa. Generally, rRNA transcript libraries contain many of the same organisms as rRNA gene libraries, indicating that most of these populations are active. Differences among total and active microbial communities correspond to waste rock geochemistry, including concentrations of sulfur, iron, and other variables such as copper, lead, and rare earth elements. Nevertheless, many of the rRNA gene and transcript sequences in these deposits were from groups without cultured representatives, and these unknown microorganisms are likely important for biogeochemical cycling over the long lifetime of these waste deposits. We also discuss recommendations for microbiological assessment of similar large historic mine waste deposits. IMPORTANCE: New Mexico has a long history of mining, with hundreds of mining districts across the state, many of which contain inactive operations with historic tailings and waste rock. Because metallurgical processing was in its infancy when most of these mines were active, they contain substantial metal resources in tailings and waste rock that could be used to support domestic demand for critical minerals. We found that microbial communities associated with these deposits do not represent typical bioleaching communities, and instead are dominated by taxa not typically associated with mine waste. However, the deposits did contain rare iron and sulfur-cycling taxa that could catalyze metal mobilization, as well as active populations of novel microorganisms that are likely important for biogeochemical cycling. These microbial communities could represent important resources for bioremediation and other biotechnological applications to recover valuable elements from these and other historic mine wastes.