Decoding Past Microbial Communities Shifts Induced by Natural and Anthropogenic Disturbance Events Through Extracellular DNA

Coastal marine ecosystems face escalating threats from multiple anthropogenic stressors, including the release of industrial contaminants. Despite decades of industrial activity impacting marine ecosystems, long-term effects on microbial communities and related key ecological functions remain unclear. Here, we analysed the prokaryotic genetic signatures of extracellular DNA preserved in sediment layers dating from the mid-17th century to the present day collected from two sites of one of the most polluted European coastal areas (i.e., Bagnoli-Coroglio Bay, Tyrrhenian Sea), where industrial activities began in the early 20th century and ended in 1992. Archaeal 16S rDNA copy numbers were higher than bacterial ones, reaching values of 2.3 and 8.8 × 107 copies during pre-industrial volcanic episodes and the intense industrial development period, respectively. Most of the archaeal genetic signatures identified along the sediment vertical profiles belong to Bathyarchaeia. The pre-industrial period showed lower diversity in terms of Amplicon Sequence Variants (ASVs) belonging to 70 prokaryotic families when compared with industrialisation periods (182 families), suggesting prokaryotic ability to respond and change in relation to modified environmental conditions occurring over time. High microbial β-diversity values were observed, with major shifts occurring for more than 50 prokaryotic taxa in both cores, suggesting that chemical contamination and volcanic eruptions fostered microbial succession, selecting certain taxa more adapted to cope with such adverse ecological conditions. Our findings indicate that extracellular DNA pools of marine sediments can hold information on long-term changes in benthic microbial diversity, representing valuable archives for understanding ecosystem dynamics over time.