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COPYRIGHTED MATERIAL Extremophiles Have Evolved to Adapt to Severe Geological Conditions

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COPYRIGHTED MATERIAL Extremophiles Have Evolved to Adapt to Severe Geological Conditions JWBS091-c01 JWBS091-Singh Printer: Yet to Come September 24, 2012 17:57 Trim: 7in × 10in 1 MOLECULAR EVOLUTION OF EXTREMOPHILES Debamitra Chakravorty Department of Biotechnology, Indian Institute of Technology, Guwahati, Assam, India Ashwinee Kumar Shreshtha Kathmandu University, Dhulikhel, Nepal V. R. Sarath Babu Max Biogen Max Fermentek Pvt. Ltd., Hyderabad, Andhra Pradesh, India Sanjukta Patra Department of Biotechnology, Indian Institute of Technology, Guwahati, Assam, India 1.1. INTRODUCTIONCOPYRIGHTED MATERIAL Extremophiles have evolved to adapt to severe geological conditions. Their adaptation cannot be justified merely as stress responses, as they not only survive but thrive in such milieus. The term extreme is used anthropocentrically to designate optimal growth for ex- tremophiles under such conditions. This can be proved through the time-evolved complexity pertaining to their molecular mechanism of adaptation. Their evolution can be mapped on the geological time scale of life, in which a thermophile is argued to be the last common ancestor from which life has arisen. The early existence of methanogens has been proved Extremophiles: Sustainable Resources and Biotechnological Implications, First Edition. Edited by Om V. Singh. © 2013 Wiley-Blackwell. Published 2013 by John Wiley & Sons, Inc. 1 JWBS091-c01 JWBS091-Singh Printer: Yet to Come September 24, 2012 17:57 Trim: 7in × 10in 2 MOLECULAR EVOLUTION OF EXTREMOPHILES by isotopic records about 2.7 Gya (gigayears ago). Extremophiles span the three domains of life and not only thrive on Earth but also occupy extraterrestrial space. One of the most im- pressive eukaryotic polyextremophiles is the tardigrade, a microscopic invertebrate found in all Earth habitats (Romano, 2003). Extremophiles such as archaea have evolved through the phenomenon of lateral gene transfer by orthologous replacement or incorporation of paralogous genes (Allers and Mevarech, 2005). It has been suggested that the switch from an anaerobic to an aerobic lifestyle by the methanogenic ancestor of haloarchaea was facil- itated by the phenomenon of lateral gene transfer of respiratory chain genes from bacteria. They also possess coregulated genes in operons, leading to coinheritance by lateral gene transfer (Allers and Mevarech, 2005). According to the 16S rRNA classification domain, archaea can be divided into four kingdoms: Crenarchaeota, Euryarchaeota, Korarchaeota, and the recently discovered Nanoarchaeota (Grant and Larsen, 1989; Huber et al., 2002). Crenarchaeota includes ther- mophiles and psychrophiles, Euryarchaeota comprises hyperthermophiles and halophiles, hyperthermophilic archaea represent Korarchaeota, and to date, Nanoarcheota is repre- sented by only a single species, Nanoarchaeum equitans. Recently, sequencing of extremophilic genomes and their global analysis has shed light on their genetic evolution. An appropriate example of such an evolutionary process is that of the radioactive damage-resistant microorganism Deinococcus radiodurans. Deinococcus possesses a robust DNA repair system that performs interchromosomal DNA recombination to cope up with radiation damage of its genome. The natural selection pressure that led to this novel evolution is known as desiccation (Cavicchioli, 2002). These organisms educate us on exactly what extremophilic evolution means. The evolutionary history of extremophiles will aid us in understanding the adaptation of microbes to extreme conditions and environments. Research on extremophiles speeded up only recently after the first genome sequence of the methanogenic archaeon Methanococcus jannaschii was published (Bult et al., 273). Success in extremophilic research is limited, due to the lack of proper in vitro conditions and genetic systems for extremophile cloning, library creation, and expression (Allers and Mevarech, 2005). Knowing the evolutionary route of extremophiles can lead to novel discoveries, adding to industrial economy. In-depth under- standing of extremophilic evolution will help in engineering extremophiles and hence add to the multibillion-dollar biotechnology industry. In this chapter we discuss the natural routes followed by extremophiles in their evolution and in ways that they can be engineered in vitro. 1.2. MOLECULAR EVOLUTION OF THERMOPHILES 1.2.1. Habitat Thermophilic environments are widespread throughout the Earth, encompassing hot springs, volcanic areas, geothermal vents and mud holes, and solfataric fields (Huber et al., 2000). They are found in several parts of the world, the largest being Yellowstone Na- tional Park in the United States. These ecosystems have high salt concentrations (3%) and slightly acidic-to-alkaline pH values (pH 5 to 8.5) (Bock, 1996). In volcanic regions large amounts of steam are formed which contain such gases as carbon dioxide, hydrogen sulfide, methane, nitrogen, carbon monoxide, and traces of ammonia or nitrate. Coal refuse piles and hot outflows from geothermal power plants constitute artificial high-temperature mi- lieus (Huber et al., 2000). Domestic and industrial hot-water systems are the anthropogenic habitats for thermophiles. JWBS091-c01 JWBS091-Singh Printer: Yet to Come September 24, 2012 17:57 Trim: 7in × 10in MOLECULAR EVOLUTION OF THERMOPHILES 3 1.2.2. Cellular Organization In the cell membranes of thermophiles, the lipid side-chain branching and ether linkages of the phosholipid bilayer contribute to their thermoadaptation (van de Vossenberg et al., 1995; Mathai et al., 2001; Futterer et al., 2004). A few extreme thermophiles such as Pyrobolus and Thermoplasma acidophilum use a modified lipid that forms a monolayer instead of a bilayer, thus making it immune to the tendency of high temperature to pull bilayers apart. In thermophiles growing above 60◦C, modifications are also observed in the metabolic pathways. Synthesis of heme, acetyl-CoA, acyl-CoA, and folic acid are either reduced or absent in thermophiles (Kawashima et al., 2000). 1.2.3. Genome Thermophilies have adapted to temperature maxima by the evolution of a wealth of structural and functional features. Recently, genomes of hyperthermophilic archaea, Nanoarchaeum equitans and Thermococcus kodakaraensis, Sulfolobus acidocaldarius, and Carboxydothermus hydrogenoformans were sequenced, providing insight into high- temperature evolution of their genome and metabolic versatility in specific thermophilic environments (Podar and Reysenbach, 2006). It has been observed that the primary structure of DNA is prone to denaturation at increased temperature by hydrolysis of the N-glycosyl bond and due to deamination of the cytosine bases (Kampmann, 2004). The genomes of such thermophiles as T. kodakaraensis show a high guanine–cytosine (GC) content (Bao et al., 2002; Saunders et al., 2003). They also show a preference for purine-rich codons, favoring charged amino acids (Paz et al., 2004). DNA shows positive supercoils in thermophiles, hence greater stability. The positive supercoils are catalyzed by the enzyme reverse gy- rase, which is present only in hyperthermophiles, in contrast to the negative supercoils in mesophiles (Madigan, 2000). Additionally, monovalent and divalent salts enhance the sta- bility of nucleic acids by screening the negative charges of the phosphate groups, protecting DNA from depurination and hydrolysis (Rothschild and Mancinelli, 2001). In some hyper- thermophiles, heat-resistant protein (histone-like protein) binds and stabilizes the DNA by lowering its melting point (Tm) (Madigan, 2000). Recently, work carried out by Zeldovich et al. (2007) concludes that an increase in purine (A + G) of thermophilic bacterial genomes due to the preference for isoleucine, valine, tyrosine, tryptophan, arginine, glutamine, and leucine, which have purine-rich codon patterns, is responsible for the possible primary adaptation mechanism for thermophilicity. These amino acid residues increase the content of hydrophobic and charged amino acids, enhancing thermostability. 1.2.4. Proteome Thermophiles are under constant threat of high temperature on their proteins. Thus, ther- mophilic intracellular protein and enzymes, compatible solutes, molecular chaperones, and translational modifications lead synergistically to their dramatic stability at high tempera- ture (England et al., 2003). Hyperthermophilic proteins are more resistant to denaturation due to restriction on the flexibility of these proteins (Scandurra et al., 1998). Factors such as increased van der Waals interactions, higher core hydrophobicity, hydrogen bonds, ionic interactions, coordination with metal ions, and compactness of proteins contribute to the- mostability (Berezovsky et al., 2007). The presence of increased salt bridges in proteins of JWBS091-c01 JWBS091-Singh Printer: Yet to Come September 24, 2012 17:57 Trim: 7in × 10in 4 MOLECULAR EVOLUTION OF EXTREMOPHILES thermophiles has been a unanimous observation claimed by many researchers (Scandurra et al., 1998). In thermophiles we also observe proline in ␤-turns, giving rise to rigidity in proteins. Change in amino acids from Lys to Arg, Ser to Ala, Gly to Ala, Ser to Thr, and Val to Ile have been observed among mesophilic to thermophilic organisms (Scandurra et al., 1998). Pertaining to secondary structure, thermostable proteins have high levels of ␣-helical and ␤-sheet content. They also have a slow unfolding rate, which helps to retain their near-native structures. For example, pyrrolidone carboxyl peptidase from Pyrococcus furiosus and ribonuclease HII from the archaeon Thermococcus kodakaraensis show slower
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