Exploring microbial growth of a model extremophile, archaeoglobus fulgidus, at elevated pressures

Abstract

Deep-sea vent and subsurface microorganisms are metabolically diverse and often display unique adaptive strategies that operate under elevated pressure conditions. However, because high hydrostatic pressure (HHP) laboratory cultivation has not been widely adopted, knowledge of how these microorganisms function in native high-pressure environments is limited. To explore how elevated pressures affect the metabolism and physiology of deep-sea and subsurface microorganisms, growth of a model extremophile, Archaeoglobus fulgidus (type strain VC16), was investigated up to 98 MPa in batch cultures for both chemoorganoheterotrophic and chemolithoautotrophic metabolisms. A. fulgidus is an anaerobic, hyperthermophilic sulfate reducing archaeon, first isolated from a shallow marine vent but has been commonly identified in high-pressure marine environments (to 2-4 km below sea level, 20-40 MPa), including deep-sea hydrothermal vents, deep geothermal wells, and deep oil reservoirs. In heterotrophic HHP cultivation experiments, exponential growth was observed up to 60 MPa. Cell densities were comparable from 0.1-40 MPa, while lower cell densities were observed at 50 MPa and 60 MPa and growth was inhibited at 70 MPa. A. fulgidus displayed both piezotolerance and moderate piezophily under certain heterotrophic HHP conditions. In autotrophic HHP conditions, A. fulgidus displayed piezotolerance with similar growth rates and maximum cell densities observed at up to 40 MPa and little to no growth was observed at 60 MPa. A. fulgidus biofilm production was observed in certain heterotrophic conditions from 0.1-50 MPa under HHP batch cultivation conditions due to both low calcium concentrations in the growth medium and the presence of a stainless steel needle that created a nucleation site. This suggests that biofilm production here was a response to growth medium chemistry and surface area, and was not related to the elevated pressure conditions. Here, A. fulgidus was shown to grow, and in some cases also produce biofilm, over a range of elevated pressure conditions. To the extent of our knowledge, piezotolerance to HHP for both heterotrophic and autotrophic metabolisms have not been previously measured for a single species. A. fulgidus’ metabolic plasticity and capacity for biofilm production reflects adaptive mechanisms that lend insight into how this species thrives in extreme and fluctuating environments.