Earth's microbial biosphere extends down through the crust and much of the subsurface, including those microbial ecosystems located within cave systems. Here, we elucidate the microbial ecosystems within anthropogenic 'caves'; the Iron-Age, subterranean tombs of central Italy. The interior walls of the rock (calcium-rich macco) were painted 2500 years ago and are covered with CaCO 3 needles (known as moonmilk). The aims of the current study were to: identify biological/geochemical/biophysical determinants of and characterize bacterial communities involved in CaCO 3 precipitation; challenge the maxim that biogenic activity necessarily degrades surfaces; locate the bacterial cells that are the source of the CaCO 3 precipitate; and gain insight into the kinetics of moonmilk formation. We reveal that this environment hosts communities that consist primarily of bacteria that are mesophilic for temperature and xerotolerance (including Actinobacteria, Bacteroidetes and Proteobacteria); is populated by photosynthetic Cyanobacteria exhibiting heterotrophic nutrition (Calothrix and Chroococcidiopsis); and has CaCO 3 precipitating on the rock surfaces (confirmation that this process is biogenic) that acts to preserve rather than damage the painted surface. We also identified that some community members are psychrotolerant (Polaromonas), acidotolerant or acidophilic (members of the Acidobacteria), or resistant to ionizing radiation (Brevundimonas and Truepera); elucidate the ways in which microbiology impacts mineralogy and vice versa; and reveal that biogenic formation of moonmilk can occur rapidly, that is, over a period of 10 to 56 years. We discuss the paradox that these ecosystems, that are for the most part in the dark and lack primary production, are apparently highly active, biodiverse and biomass-rich.
The moonmilk is a secondary calcite deposit (speleothem) formed by nanofibers of calcite and commonly found in karst caves. While its biogenic origin is widely accepted, the mechanism of calcite nanofibers production remains unclear. Crystallization and formation mechanism of calcium carbonate nanostructures are of high interest in different fields, such as geomicrobiology (rock-microbes interactions), astrobiology (biosignatures), medicine (antibiotics producing bacteria), nanotechnology (calcium carbonate nanofibers) and recently, archeology. The discovery of the moonmilk in the hypogeal tombs of the ancient necropolis of Tarquinia (Italy), provides a unique opportunity to compare moonmilk crystal shapes that originated from two type of rocks, Macco (a calcarenite) and Sabbione (a hybrid sandstone). We analyzed, through a SEM analysis, moonmilk samples from twelve tombs in the necropolis area and found that rocks provide an ideal environment for the formation of the nanofibers; the Sabbione promoted the growth of a finer and thinner carbonate nanostructures, probably due to a slower growth kinetics caused by a low calcium value present in this rock.
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