Abstract

High hydrostatic pressure (HHP) batch cultivation of a model extremophile, Archaeoglobus fulgidus type strain VC-16, was performed to explore how elevated pressures might affect microbial growth and physiology in the deep marine biosphere. Though commonly identified in high-temperature and high-pressure marine environments (up to 2–5 km below sea level, 20–50 MPa pressures), A. fulgidus growth at elevated pressure has not been characterized previously. Here, exponential growth of A. fulgidus was observed up to 60 MPa when supported by the heterotrophic metabolism of lactate oxidation coupled to sulfate reduction, and up to 40 MPa for autotrophic CO2 fixation coupled to thiosulfate reduction via H2. Maximum growth rates for this heterotrophic metabolism were observed at 20 MPa, suggesting that A. fulgidus is a moderate piezophile under these conditions. However, only piezotolerance was observed for autotrophy, as growth rates remained nearly constant from 0.3 to 40 MPa. Experiments described below show that A. fulgidus continues both heterotrophic sulfate reduction and autotrophic thiosulfate reduction nearly unaffected by increasing pressure up to 30 MPa and 40 MPa, respectively. As these pressures encompass a variety of subsurface marine environments, A. fulgidus serves as a model extremophile for exploring the effects of elevated pressure on microbial metabolisms in the deep subsurface. Further, these results exemplify the need for high-pressure cultivation of deep-sea and subsurface microorganisms to better reflect in situ physiological conditions.

Highlights

  • High hydrostatic pressure (HHP) is an inherent characteristic of all deep marine ecosystems (e.g., Jannasch and Taylor, 1984; Oger and Jebbar, 2010; Picard and Daniel, 2013), which are anchored by diverse microbial communities of primary producers and consumers

  • Studies of microbial responses to high pressure can be divided into those that focus on the potentially deleterious effects of pressure on surface species, and the adaptation mechanisms of piezotolerant and piezophilic organisms. Those species that are negatively impacted by highpressure conditions are categorized as piezosensitive, while piezotolerant species are insensitive to high pressure up to a limit; piezophiles grow optimally at elevated pressure and some of these are incapable of growth at ambient pressure

  • The maximum growth rate for experiments that used the syringebased HHP techniques was observed at 20 MPa (0.15 ± 0.005 hr−1, Figure 3C), while the growth rate at 0.1 MPa was 0.13 ± 0.008 hr−1 (Figure 3C), suggesting that A. fulgidus is a moderate piezophile under these conditions

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Summary

Introduction

High hydrostatic pressure (HHP) is an inherent characteristic of all deep marine ecosystems (e.g., Jannasch and Taylor, 1984; Oger and Jebbar, 2010; Picard and Daniel, 2013), which are anchored by diverse microbial communities of primary producers and consumers. Studies of microbial responses to high pressure can be divided into those that focus on the potentially deleterious effects of pressure on surface species, and the adaptation mechanisms of piezotolerant and piezophilic organisms By definition, those species that are negatively impacted by highpressure conditions are categorized as piezosensitive, while piezotolerant species are insensitive to high pressure up to a limit; piezophiles grow optimally at elevated pressure and some of these are incapable of growth at ambient pressure (obligate piezophiles; e.g., Jannasch and Taylor, 1984; Kato et al, 2008; Fang et al, 2010). While these categories are traditionally applied at the strain level, the pressure response can vary within a strain as other growth conditions vary (e.g., metabolism, temperature, energy supply; Nogi et al, 1998; Zhao et al, 2015)

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