Microbial communities differ in warm and cold periods over >150,000 years

Glacier-archived records are powerful windows into past climates and ecosystems, but variation in co-preserved microbiota is rarely characterized over long time periods or connected to changing climates. In a 310-meter ice core from the Guliya ice cap, Tibetan Plateau, we linked microbial communities to concomitant climatic conditions across 33 depths, spanning at least the last 150,000 years. Communities differed significantly between cold and warm periods, and among the three major climate epochs Holocene, Last Glacial Stage (LGS), and Pre-LGS. Although source inputs varied during these periods, the microbial changes appeared independently impacted by climate as well. Co-occurrence network analyses suggested the importance of glacial surface-growing communities, and their phototrophs, to the preserved microbial record. The inferred microbial growth (by cell densities, diversity, and potential doubling times pre-compaction into solid ice) on Guliya’s surfaces was higher during cold periods than warm periods, likely associated with deeper snow and firn layers under colder conditions. Three Cyanobacteria “blooms” were captured in the record, and were significantly correlated to overall microbial concentration and diversity, as well as the abundance of two heterotrophic photosynthetic clades (the genus Geodermatophilus and the class Chloroflexia). Taxonomically, 6 genera were historically persistent and dominant throughout the record (Polaromonas, Flavobacterium, Massilia, Aquaspirillum, Pedobacter, and Cryobacterium), one of which (Cryobacterium) exhibited a shift in dominant strains from the Pre-LGS to the LGS, indicating a possible speciation event. Collectively, these findings advance our understanding of ancient glacier-archived microbial communities and the ecological forces they experienced, provide evidence for microbiological responses to the prevailing climate regime, and may shed new light on the microbial evolution across a long-term history over at least the last >150,000 years.