Life on the edge: Microbial biomineralization in an arsenic- and lead-rich deep-sea hydrothermal vent

Abstract

Unravelling complex microbial activity in modern hydrothermal vents can provide crucial insights into the evolution of ancient life on Earth. It is well established that microorganisms in hydrothermal vents have a significant impact on the cycling of metals and mineral formation. However, the detailed roles played by microorganisms in driving sulfide deposition and cycling of toxic metals, like arsenic (As) and lead (Pb), in high-temperature deep-sea hydrothermal vents remain unknown. The understanding of these mechanisms in extreme environments is of particular importance as As has been postulated as a driver of microbial activities on the early Earth. Here, we present the first geologic evidence of PbAs rich microbial filamentous clusters observed in a modern high-temperature black smoker from the Manus back-arc basin, Papua New Guinea. The clusters occur as net-like structures on the surface of barite and sulfides and are composed of multiple filaments and fine-grained PbAs sulfosalt. Each of the filaments includes an As-Pb-rich sulfosalt core and organic-rich shell structure with elevated carbon, nitrogen and phosphorus. Further synchrotron X-ray absorption near edge structure analysis shows that the clusters contain a mixture of As (II) and As (III). Additionally, those filaments show a close association with realgar (As4S4), by penetrating and dissolving this As-sulfide mineral. We interpret the filaments to be a result of As-related microbial activity in As- and Pb-enriched hydrothermal environments. The findings show possible processes through which extremophiles live in Pb and As-rich environments during chimney growth. In addition, as hydrothermal vents are regarded as modern analogs of ancient volcanogenic massive sulfide deposits, the observed biominerals present the potential to be used as proxies to trace the signatures of early life in ancient geological systems.