The Molecular Basis for Life in Extreme Environments

Abstract

Sampling and genomic efforts over the past decade have revealed an enormous quantity and diversity of life in Earth's extreme environments. This new knowledge of life on Earth poses the challenge of understanding its molecular basis in such inhospitable conditions, given that such conditions lead to loss of structural changes and of function in biomolecules from mesophiles. In this review, we discuss the physicochemical properties of extreme environments. We present the state of recent progress in extreme environmental genomics. We then present an overview of our current understanding of the biomolecular adaptation to extreme conditions. As our current and future understanding of biomolecular structure–function relationships in extremophiles requires methodologies adapted to extremes of pressure, temperature, and chemical composition, advances in instrumentation for probing biophysical properties under extreme conditions are presented. Finally, we briefly discuss possible future directions in extreme biophysics. Expected final online publication date for the Annual Review of Biophysics, Volume 50 is May 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Structural Evolution of the Ancient Enzyme, Dissimilatory Sulfite Reductase

“…Together these studies suggest that Dsr likely emerged to catalyze SO 3 2reduction and then diversified (through recruitment of APS and Sat) to catalyze SO 4 2reduction and ultimately HSoxidation (9)(10)(11)(12). The phylogenetic studies conducted herein suggest that model bacterial SROs implicated as major players in contemporary biogeochemical S cycling (e.g., Deltaproteobacteria and Firmicutes) evolved comparatively recently whereas early evolving archaeal SROs (and a few taxonomically patchy bacterial genera) tend to be restricted to hydrothermal or more nutrient-limited extreme environments (11) where oxidant limitation is likely pervasive (50). While the ecological drivers of the evolution of SROs (via Dsr phylogeny) is obscured in the present study by limited corresponding metadata (e.g., cardinal growth parameters, geochemistry) associated with these organisms or the environments from where they were recovered, the broad differences in habitats of early evolving and later evolving SROs suggests that the ecology of Dsr-harboring SROs has evolved over time.…”

“…While this proposed pathway warrants experimental scrutiny, the co-evolution at the positions putatively involved also indicates that this pathway was likely established prior to the radiation of all DsrAB, although the precise residues involved in these interactions vary across Dsr enzyme types. Consequently, the presence of a slightly modified allosteric pathway may have allowed fine-tuning of Dsr activity in the context of different physiological backgrounds, including those that operate under chronic energy (dissimilatory eshuttling) stress imposed by extreme conditions (e.g., temperature, pH and pressure) (50) where the kinetics of HSO 3 reduction and thus growth of SRO are likely to be much slower. The combination of the evolutionary coupling analysis and ANM dynamic "normal mode" calculations provide an intriguing set of residues to probe for their involvement in structure-function relationships in future experiments.…”

Structural Evolution of the Ancient Enzyme, Dissimilatory Sulfite Reductase

“…Together these studies suggest that Dsr likely emerged to catalyze SO 3 2- reduction and then diversified (through recruitment of APS and Sat) to catalyze SO 4 2- reduction and ultimately HS-oxidation (9–12). The phylogenetic studies conducted herein suggest that model bacterial SROs implicated as major players in contemporary biogeochemical S cycling (e.g., Deltaproteobacteria and Firmicutes) evolved comparatively recently whereas early evolving archaeal SROs (and a few taxonomically patchy bacterial genera) tend to be restricted to hydrothermal or more nutrient-limited extreme environments (11) where oxidant limitation is likely pervasive (47). While the ecological drivers of the evolution of SROs (via Dsr phylogeny) is obscured in the present study by limited corresponding metadata (e.g., cardinal growth parameters, geochemistry) associated with these organisms or the environments from where they were recovered, the broad differences in habitats of early evolving and later evolving SROs suggests that the ecology of Dsr-harboring SROs has evolved over time.…”

“…While this proposed pathway warrants experimental scrutiny, the co-evolution at the positions putatively involved also indicates that this pathway was likely established prior to the radiation of all DsrAB, although the precise residues involved in these interactions vary across Dsr enzyme types. Consequently, the presence of a slightly modified allosteric pathway may have allowed fine-tuning of Dsr activity in the context of different physiological backgrounds, including those that operate under chronic energy (dissimilatory e - shuttling) stress imposed by extreme conditions (e.g., temperature, pH and pressure) (47) where the kinetics of HSO 3 - reduction and thus growth of SRO are likely to be much slower. The combination of the evolutionary coupling analysis and ANM dynamic “normal mode” calculations provide an intriguing set of residues to probe for their involvement in structure-function relationships in future experiments.…”

Experimental study of proteome halophilicity using nanoDSF: a proof of concept

“…In particular, in extreme environments, organisms thrive under 63 permanent extreme conditions and their proteins face considerable physical and chemical 64 challenge. However, it is now clear that protein adaptation is tightly associated with 65 environmental adaptation, especially for extremophiles (Reed et al 2013;Singh et al 2020; 66 Ando et al 2021). Notably, comparative studies between homologous proteins of organisms 67 isolated from various environments are useful for assessing the degree of adaptation of an 68 organism to various conditions (Coquelle et al 2010;Dick et al 2016).…”