Halophilic Bacteria and Their Biomolecules: Recent Advances and Future Applications in Biomedicine
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Mor. J. Agri. Sci. 1(6): 323-335, December 2020 323 Halophilic bacteria and their biomolecules: Recent advances and future applications in biomedicine Naima BOU MHANDI1 Abstract The organisms thriving under extreme conditions better than any other organism living on Earth fascinate by their hostile growing parameters, physiological features and their 1 Specialized Center of Valoriza- tion and Technology of Sea production of valuable bioactive metabolites. This is the case of halophilic bacteria that Products, National Institute grow optimally at high salinities and are able to produce biomolecules of pharmaceutical of Fisheries Research, Agadir, interest for therapeutic applications. As long as the microbiota is being approached by mas- Morocco sive sequencing, novel insights are revealing the environmental conditions in which the compounds are produced in the microbial community without more stress than sharing the same salt substratum with their peers. In this review are reported the molecules produced * Corresponding author [email protected] by halophilic bacteria with a spectrum of action in vitro: antimicrobial and anticancer. The action mechanisms of these molecules, the urgent need to introduce alternative lead Received 21/12/2020 compounds and the current aspects on the exploitation and its limitations are discussed. Accepted 30/12/2020 Keywords: Halophilic bacteria, biomolecules, biomedicine, antimicrobial INTRODUCTION Ventosa et al., 2004; Amoozegar et al., 2016). Extremely halophilic bacteria generally grow slowly. Halophilic Halophiles are organisms represented by archaea, bacte- bacteria can be identified commonly by phenotypic ria and eukarya for which the main characteristic is their characterization as well as 16S rRNA gene sequences salinity requirement, halophilic “salt-loving”. Halophilic (Fendrihan et al., 2012). Moderately halophilic bacteria microorganisms constitute the natural microbial com- are dominant in mostly hypersaline environments and munities of hypersaline ecosystems, which are widely they constitute a major proportion of total microbial distributed around the world (Oren, 2008). They require population in the hypersaline environments and play a sodium ions for their growth and metabolism. Thus, major ecological role. based on the NaCl optimal requirement for growth, the halophiles are classified in three different categories: Currently, a large number of bacterial species related slight (1–3%); moderate (3–15%) and extreme (15– to different bacterial phyla, especially gram-positive, 30%) (Kushner, 1978; Kushner and Kamekura, 1988). In showed moderately halophilic response. Moderately contrast to halotolerant organisms, obligate halophiles halophilic bacteria include members of Proteobacteria require NaCl concentrations higher than 3% NaCl or (Halomonas, Chromohalobacter, Pseudomonas, Ma- above of seawater, with about 3.5% NaCl (Rodriguez- rinobacter, Rhodospirillum, Aeromonas, Alteromonas, Valera et al, 1981). The tolerance parameters and salt Rhodovibrio, Halovibrio and Alcaligenes), Firmicutes requirements are dependent on temperature, pH and (Halobacillus, Virgibacillus, Oceanobacillus, Staphylo- growth medium. In this way, the halophiles are adapted coccus, Gracilibacillus, Clostridium, Pontibacillus, Spo- and limited by specific environmental factors. Those -mi rosarcina and Planococcus), Actinobacteria (Kocuria, croorganisms able to survive and optimally thrive under Streptomyces and Rubrobacter), Actinomycetes (Nocar- a wide spectrum of extreme environmental factors are dia, Nocardiopsis, Streptomonospora, Actinopolyspora designated as poly-extremophiles (Seckbach et al., 2013; and Nesterenkonia) and Bacteriodetes (Flavobacterium, Bowers et al., 2009). In fact, a halophilic microorganism Salinibacter and Polaribacter). can also be alkaliphile, designated as haloalkaliphile, Mostly, extreme halophilic bacteria contain a variety of growing optimally or very well at pH values above 9.0, carotenoids as carotenoids help membrane stabilization but cannot grow at the near neutral pH value of 6.5 in Thermus thermophiles, Ruberobacter radiotolerans (Mesbah and Wiegel, 2012). and help to tolerate the high osmotic stress in Halobacte- Halophilic bacteria are cocci, rod, triangular and even rim spp. (Amoozegar et al., 2016, Fendrihan et al., 2012, square-shaped. Some strains are pleiomorphic especial- Sasaki et al., 2012) Many gram-positive bacteria isolated ly when the ionic conditions of the media are altered and from different saline environments (salt lakes, salt mines most lie below the NaCl level of 1M/L. The physiology of and salt marshes) also have carotenoids which indicate the moderate and extreme halophilic bacteria is affected the crucial role of carotenoids in osmotolerance of these by change in salt concentration, growth temperature bacteria (Ii et al., 2015). and nature of available nutrients (Fourcans et al., 2006; © Moroccan Journal of Agricultural Sciences • e-ISSN: 2550-553X www.techagro.org 324 Bou Mhandi: Halophilic bacteria and their biomolecules Cyanobacteria are characterized by the presence of chlo- In this review, we focus on the biomolecules described rophyll and phycobilin pigments. They are photosyn- as antimicrobial or anticancer compounds produced thetic bacteria (planktonic biomass) and form microbial by halophilic bacteria and discuss current and future mats in many hypersaline lakes (Baxter et al., 2014). perspectives in this field. Aphanothece halophytica is an extreme halophile form of brown layer of microbial mat on the water surface. Most ANTIMICROBIAL COMPOUNDS cyanobacteria use glycine betaine as the major compat- ible solute which they take from the medium or synthe- The current situation of antibiotic resistance propaga- size from choline (Boornburapong et al., 2016). Many tion poses a global threat to public health. Over the past genera related to halophilic cyanobacteria have been decades, antibiotics have saved millions of lives, but their described from the Dead Sea, the Great Salt Lake, Solar misuse has led to the emergence of multi-drug resistant Lake and other salt lakes and ponds but the cyanobacte- bacteria (MDR), reducing or nullifying their effective- rial diversity has not been studied extensively from the ness. Recently, the continuous increase in antibiotic hypersaline environments (Tripathi et al., 2013). Moder- resistance is reaching critical levels, which implies an ately halophilic purple sulfur bacteria like Chromatium increase in morbidity in the healthy population and an spp. have the ability to store sulfur granules inside cells imminent risk for hospitalized patients (Tseng et al., and they grow phototrophically by using glycerol or gly- 2018; Peters et al., 2019). In fact, the main cause of death colate. Rhodospirilum salexigens (purple non-sulfur bac- of patients are attributable to complications due to MDR terium) can use glycine, betaine or ectoine as osmolytes. infections (Cassini et al., 2019). Preventing the return Sulfur oxidizing bacteria are halophilic gram-positive, to the pre-antibiotic era is one of the main challenges for science. The urgent need to introduce new effective filamentous CO2 fixing bacteria. They oxidize sulfur and hydrogen sulfide to form sulfates. For example, Achro- antimicrobial therapies is leading to the exploitation of matium volutans, a filamentous bacterium was isolated all possible natural and sustainable resources, including from solar lakes and Thiobacillus halophilus a halophilic extreme environments as a promising resource for new chemoauthotrpohic bacterium was isolated from the antibiotic discovery. The first antimicrobial compounds hypersaline lake, Australia (Sorokin et al., 2014). from halophilic microorganisms were reported in 1982 by Rodriguez-Valera et al. (1982). Halocin was the term BIOTECHNOLOGICAL IMPORTANCE OF coined for substances secreted by several members of the genus Halobacterium capable of causing death and lysis HALOPHILIC BACTERIA of the surrounding microbiota. Halocins are the pro- The exploitation of extremophiles is having special teins and antimicrobial peptides (AMPs) produced by importance in the development of new molecules with haloarchaea (Rodriguez-Valera et al., 1982; Gohel et al., potential applications in biomedicine. Current efforts 2015). Despite the ecological and environmental role of are focused primarily to cover the urgent health needs, several halocins, their action against human pathogens especially those that represent the main global threats, has been less studied. In the fight against time, the clini- cancer and antibiotic resistance. The great metabolic cal significance of halophilic microorganisms is minorly versatility of halophilic microorganisms, their low nu- reported and the antimicrobial action against the most tritional requirements and their genetic machineries of important risk group of human pathogens ESKAPE: adaptation to harsh conditions, like nutrient starvation, Enterococcus faecium, Staphylococcus aureus, Klebsiella desiccation, high sun radiation, and high ionic strength, pneumoniae, Acinetobacter baumannii and Pseudomo- make them promising candidates and a hope for drug nas aeruginosa, still remains as a potential. According to discovery (Charlesworth and Burns, 2015). Continuous the data inferred, the antagonistic action identified and advances in “omics” and bioinformatic tools are reveal- the production of bioactive compounds by halophilic ing uncountable encoding genes for the production of microorganisms are derived