Stochastic seeding and environmental stressors as dual drivers of pioneer microbial colonization in newly formed basaltic lava tubes

Abstract

Lava tubes formed during the 2021 Tajogaite eruption on La Palma (Canary Islands, Spain) provide a rare opportunity to investigate the earliest stages of microbial colonization in a newly created subterranean volcanic environment. Although microbial communities in volcanic terrains have been widely studied, the first colonizers of newly formed lava tubes and their interactions with new mineral surfaces remain poorly understood. Here, we combined microscopy, mineralogy, stable isotope analysis, culture-dependent techniques, and 16S rRNA gene high-throughput sequencing to characterize mineral substrates, microenvironmental parameters and pioneer microbial communities 12–24 months after lava tube formation. Microbial assemblages were dominated by bacteria from the Actinomycetota, Bacillota, and Pseudomonadota phyla, together with archaea from the Methanobacteriota phylum. Organic debris from animals (notably seabirds and rodents) likely contributed to early microbial seeding and community development, as indicated by the detection of host-associated and opportunistic bacteria (e.g., Staphylococcus, Sphingomonas, Pseudomonas). Biofilm-like structures and extracellular polymeric substances were observed in association with sodium-rich sulfate and carbonate minerals, suggesting incipient microbe-mineral interactions during early mineral weathering. Archaeal-enriched communities adapted to highly saline and oligotrophic substrates (e.g., Halostagnicola, Halonotius, and Halorubrum) in some of these nascent tubes further support environmental filtering by microhabitat geochemistry and mineralogical context during early community assembly. Our findings indicate that early microbial colonization is initiated by stochastic seeding processes (via aerosols, animals, or atmospheric inputs), whereas environmental stressors related to volcanic degassing, ventilation, and extreme geochemical conditions act as strong deterministic filters that shape the final community structure in newly formed basaltic lava tubes, as reflected by the significant role of δ13C–CO2.