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Extremophile Microbial Communities and Enzymes for Bioenergetic App- Lication Based on Multi-Omics Tools Send Orders for Reprints to [email protected] 240 Current Genomics, 2020, 21, 240-252 MINI REVIEW ARTICLE Extremophile Microbial Communities and Enzymes for Bioenergetic App- lication Based on Multi-Omics Tools Gislaine Fongaro1, Guilherme Augusto Maia1, Paula Rogovski1, Rafael Dorighello Cadamuro1, Joana Camila Lopes1, Renato Simões Moreira1, Aline Frumi Camargo2, Thamarys Scapini2, Fábio Spitza Stefanski2, Charline Bonatto2,3, Doris Sobral Marques Souza1, Patrícia Hermes Stoco1, Rubens Tadeu Delgado Duarte1, Ariadne Cristiane Cabral da Cruz4, Glauber Wagner1 and Helen Treichel2,* 1Department of Microbiology, Immunology, and Parasitology, Federal University of Santa Catarina, Florianópolis, SC, Brazil; 2Laboratory of Microbiology and Bioprocess, Federal University of Fronteira Sul, Erechim, RS, Brazil; 3Department of Chemical and Food Engineering, Federal University of Santa Catarina, Florianópolis, SC, Brazil; 4Department of Dentistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil Abstract: Genomic and proteomic advances in extremophile microorganism studies are increasingly demonstrating their ability to produce a variety of enzymes capable of converting biomass into bioen- A R T I C L E H I S T O R Y ergy. Such microorganisms are found in environments with nutritional restrictions, anaerobic envi- Received: January 10, 2020 ronments, high salinity, varying pH conditions and extreme natural environments such as hydrother- Revised: February 02, 2020 mal vents, soda lakes, and Antarctic sediments. As extremophile microorganisms and their enzymes Accepted: April 20, 2020 are found in widely disparate locations, they generate new possibilities and opportunities to explore DOI: biotechnological prospecting, including biofuels (biogas, hydrogen and ethanol) with an aim toward 10.2174/1389202921999200601144137 using multi-omics tools that shed light on biotechnological breakthroughs. Keywords: Biodiversity, microorganisms, enzymes, molecular methods, multi-omics, extremophiles. 1. MICROBIAL COMMUNITIES IN EXTREME EN- Extremophiles are classified in categories based on envi- VIRONMENTS – AN INTRODUCTION ronmental parameters, with sub-definitions created to ac- commodate organisms that present moderate, extreme, hy- From a human point of view, some habitats seem so per-extreme and also obligate extremophile (Table 1). harsh and inhospitable for life that they are commonly thought to be sterile. The > 85°C hot springs in the Yellow- Comparative studies between extremophiles and their stone Park (USA), the ultra-arid Atacama Desert (Chile), and non-extreme counterparts have led to systematic descriptions the permanent glacier ice of South Pole (Antarctica) repre- of how growth and survival are possible under extreme con- sent some examples. These “extreme” environments, howev- ditions. In general, extremophiles adjust their membranes, er, are dominated by microbial cells from all three domains proteins and nucleic acids to preserve the functional stability of life: Bacteria, Archaea, and Eukarya. Microorganisms of their structures and molecular components [4, 5]. To inhabiting such environments are called “extremophiles” achieve this stability, several strategies evolved as microor- because of their endemic (or restricted) nature to survive at ganisms were exposed to environmental stresses. For exam- the edge of life [1]. Extremophiles exhibit unusual biochem- ple, to maintain their metabolism under extreme cold, psy- ical and ecological adaptations not found by organisms chrophiles must resist freezing and, at the same time, con- dwelling in no-extreme habitats. Physical and chemical pa- serve membrane flexibility. These cold-adapted microorgan- rameters in the extreme environments include a broad range isms enriched their membranes with unsaturated fatty acids of temperature (from –40 to >130°C), salinity (from rainwa- that provide flexibility, and present enzymes enriched in ter to 5 M NaCl), pH (from virtually 0 to 13), pressure (from hydrophilic amino acids (e.g., glycine) that help retains liq- 0.3 atm at Mount Everest to 1200 atm in the deepest point of uid water for metabolism [6]. Mariana Trench), desiccation (from wet to the complete ab- Virtually all extremophiles present enzymatic adaptations sence of water), and radiation (wavelengths of ultraviolet and to cope with their unusual environments. As enzymatic func- gamma rays) [2, 3]. tion depends on temperature, pH and water availability, for example, all intra- and extracellular reactions rely on adapta- tions of extremophilic enzymes-also known as “extrem- *Address correspondence to this author at the Laboratory of Microbiology ozymes”. While performing the same enzymatic functions as and Bioprocess, Federal University of Fronteira Sul, Erechim, RS, Brazil; Tel/Fax: +55 54981126456; E-mail: [email protected] their non-extreme counterparts, extremozymes catalyze 1389-2029/20 $65.00+.00 ©2020 Bentham Science Publishers Extremophile Microbial Communities and Enzymes for Bioenergetic Application Current Genomics, 2020, Vol. 21, No. 4 241 chemical reactions in conditions that would completely in- Using metagenomic analysis is possible to evaluate the hibit or even denature other enzymes [7]. In fact, some of thermophile community composition by sequencing markers these enzymes display a phenomenon known as polyex- like 16S rRNA [25, 26], however, analyzing the whole DNA tremophilicity, i.e., they present activity in several extreme of these communities by shotgun metagenome strategy, the conditions. For example, biochemical analysis of an alcohol potential functionality of the microbiome may be addressed dehydrogenase from the hyperthermophilic archaea Thermo- and also identify coding genes that play an important role in coccus sibiricus showed activity at high temperatures (opti- metabolic route with biotechnological interest or genes with mal close to 100°C) and high salt concentrations (4 M NaCl) unknown function [19, 27, 28]. [8, 9]. These unique features from extremophiles and their Besides metagenomics data and complete genome se- enzymes opened a myriad of applications in bioprocesses quences from different species widely available and led to and bioenergy research [7, 10]. discover new genes, transcriptome and proteome techniques are very useful not only to identify the expressed genes but 2. EXTREMOZYMES AND MULTI-OMIC TOOLS also to understand their expression with certain conditions Extremozymes are enzymes obtained from extremophile and the physiological responses of these conditions [29-31]. Although the metatranscriptome is very useful to provide microorganisms that have several ecological roles in envi- insights about the transcriptional activity of certain environ- ronment and succession, being a rich niche to be explored mental conditions [18, 32], the mRNA and protein expres- considering enzymes and other molecules [11]. The biodeg- sions could not be directly correlated because of the post- radability and high stability of extremozymes have been ex- transcription regulations [33]. However, metaproteomic ploited in a large range of industrial applications with vari- analysis is usually less restrictive and can offer rapid physio- ous tolerances, including acid, cold, salt and alkali-tolerant logical responses since protein expression is modulated very enzymes [12, 13]. Due to its catalytic capability, enzymes fast. In addition, metaproteomics analysis has some im- have been widely applied for industrial purposes, the pro- portant bias, which depends on the protein extraction and spection of enzymes market is in increasing growth. In 2004, separation methods [34]. it was estimated at $2 billion dollars; in 2010, the value in- Though the combination of metagenome, metatranscrip- creased to $3.3 billion; and in 2018, the estimated value of tome and metaproteomics could bring more evidence of the this market was $7.1 million [14-16]. functionality and expression of certain enzymes with bio- With the advancement of "omics" technologies, the de- technological interest [18], these studies with extremophile velopment of new bioinformatics tools is possible to estimate microbial communities are scarce in the literature, especially the microbial composition communities and also understand because this is still a developing field. A study of Mandelli et the functional aspects of these communities and prospecting al. [35] performed a multi-omic approach with the extremo- genes and enzymes with a desirable characteristic or func- phile Thermus filiformis using DNA sequencing, RNA-Seq tionality [17-19]. Thus, metagenomic [20, 21], meta- and mass spectrometry. They considered that the multi-omic transcriptomic [22] and metaproteomic [23, 24] are interest- analyses were complementary to each other and allowed ing strategies to prospect and study these enzymes and their them to identify the main changes in the physiological state role in extremophile communities. This variety of strategies of T. filiformis under varying temperatures. The authors also can be used to identify molecular mechanisms or metabolic discovered several thermostable macromolecules produced routes with possible industrial applications of microorgan- by T. filiformis, including amylases, pyrophosphatases, glu- isms and enzymes (Fig. 1). cosidases, and galactosidases, all of which have a wide range of biotechnological and industrial applications. Table 1. Classification of extremophiles according to environmental parameters. Environmental Parameter Classification Definition
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