Abstract

Recent studies have uncovered a vast number of thermophilic species in icy environments, permanently cold ocean sediments, cold sea waters, and cool soils. The survival of thermophiles in psychrobiotic habitats requires thorough investigation of the physiological and molecular mechanisms behind their natural cryopreservation. Such investigations are mainly impeded due to a restricted cultivation of thermophiles at low temperatures under the laboratory conditions. Artificial culture media used under the laboratory conditions usually fail to support cultivation of thermophiles at low-temperature range. In this study we cultivated the extreme thermoacidophilic archaeon Metallosphaera sedula with the preliminary powdered and sterilized multimetallic extraterrestrial mineral material (the meteorite NWA 1172) under a low temperature regime in laboratory conditions. Our data indicate that M. sedula withstands cold stress and can be maintained at low temperatures, when supplemented with the meteorite NWA 1172 as the sole energy source. Cultivation with the meteorite NWA 1172 opens up new, previously unknown psychrotolerant characteristics of M. sedula, emphasizing that culture conditions (i.e., the nutritional environment) may affect the microbial survival potential in stress related situations. These observations facilitate further investigation of strategies and underlying molecular mechanisms of the survival of thermophilic species in permanently cold habitats.

Highlights

  • Diverse extremophilic microorganisms have been discovered in habitats characterized by parameters that go beyond the range of their physiological activity

  • We show that the extreme thermoacidophile Metallosphaera sedula is among a very few thermophiles supported at cold temperatures under laboratory conditions

  • M. sedula has been described as a well-defined, obligate thermophile which requires a temperature range from 50 to 80◦C for growth, with an optimum of 73◦C (Huber et al, 1989; Auernik et al, 2008)

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Summary

Introduction

Diverse extremophilic microorganisms have been discovered in habitats characterized by parameters that go beyond the range of their physiological activity. M. sedula at Cold Temperatures in icy habitats (Bulat et al, 2004; Lavire et al, 2006; Bulat, 2016; Papale et al, 2019; Gura and Rogers, 2020); permafrost environments (Gilichinsky et al, 2007; Demidov and Gilichinsky, 2009; Mironov et al, 2010; Shcherbakova et al, 2011); cool soils with temperatures constantly below 25◦C (Marchant et al, 2002, 2008, 2011; Rahman et al, 2004; Zeigler, 2014); “arctic thermophiles” in permanently cold (−2◦ to 4◦C) ocean sediments (Hubert et al, 2009, 2010; de Rezende et al, 2013; Müller et al, 2014; Robador et al, 2016; Bell et al, 2018, 2020; Chakraborty et al, 2018); and non-spore-forming hyperthermophiles in cold (2–4◦C) seawater (Huber et al, 1990; Wirth, 2017) How these thermophilic species, abundantly represented in permanently cold habitats, can tolerate low temperatures significantly below their minimum requirement for growth is an intriguing subject of current investigations. It has been suggested that microorganisms capable of growth in temperature range of both thermobiotic and mesobiotic environments may contain two different sets of key enzymes whose synthesis are regulated by temperature (Wiegel, 1990)

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