A review on enzymatic response to salt stress and genomic/metagenomic analysis of adaptation protein in hypersaline environment.

Habeebat Adekilekun Oyewusi, Muhammad Muhammad, Roswanira Abdul Wahab, Fahrul Huyop

Abstract


Microorganisms adapted to conditions of high salinity (low water activity) provide an understanding on how the problem of maintaining an efficient cell integrity under high osmotic stress conditions that had been tackled naturally. Almost all microbes adapting to extreme situations either by intracellularly amass inorganic ions (K+) to counterbalance high salt concentration or by synthesizing and accumulating certain organic solutes called compatible solutes that confer protection without affecting cell functions and this process may be chloride ion dependent in some microorganisms. However, the use of culture-independent method like genomic or metagenomics shields more light on the microbial diversity, gene structure and regulation as well as discovery of novel genes that led to understanding of their adaptation mechanism and roles in extreme environments. Therefore, microbes that survive this natural attenuation aimed at acclimatizing with the extreme environments could serve as the sources of biotechnologically essential molecules with an extensive array of uses.


Keywords


Enzymatic response; genomic analysis; hypersaline environments; metagenomic; salt stress.

Full Text:

PDF PDF

References


Alavi, S., Rafieyan, S., Yavari-Bafghi, M., & Amoozegar, M. A. (2020). Extremophiles: A Powerful Choice for Bioremediation of Toxic Oxyanions. In Microbial Bioremediation & Biodegradation (pp. 203-249). Springer, Singapore.

Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R., & Stahl, D. A. (1990). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol., 56(6), 1919-1925.

Antón, J., Oren, A., Benlloch, S., Rodríguez-Valera, F., Amann, R., and Rosselló-Mora, R. (2002). Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. International Journal of Systematic and Evolutionary Microbiology, 52(2), 485-491

Antunes, A., Olsson-Francis, K., & McGenity, T. (2020). Exploring deep-sea brines as potential terrestrial analogues of oceans in the icy moons of the outer solar system. Curr. Issues Mol. Biol.

Asante, J., & Osei Sekyere, J. (2019). Understanding antimicrobial discovery and resistance from a metagenomic and metatranscriptomic perspective: advances and applications. Environmental microbiology reports, 11(2), 62-86.

Avci, M. K., Yamaner, C., Ayvaz, M., & Yazgan-Karatas, A. (2014). In silico characterization and comparative analysis of Bacillus subtilis GntR type LutR transcription factor. EurAsian Journal of BioSciences, (8).

Avonce, N., Mendoza-Vargas, A., Morett, E., & Iturriaga, G. (2006). Insights on the evolution of trehalose biosynthesis. BMC Evolutionary Biology, 6(1), 109.

Baker, J. L., Lindsay, E. L., Faustoferri, R. C., To, T. T., Hendrickson, E. L., He, X., Shi, W., McLean, J.S., & Quivey, R. G. (2018). Characterization of the trehalose utilization operon in Streptococcus mutans reveals that the TreR transcriptional regulator is involved in stress response pathways and toxin production. Journal of Bacteriology, 200(12), e00057-18.

Bakka, K., & Challabathula, D. (2020). Amelioration of Salt Stress Tolerance in Plants by Plant Growth-Promoting Rhizobacteria: Insights from “Omics” Approaches. In Plant Microbe Symbiosis (pp. 303-330). Springer, Cham.

Baliga, N. S., Bonneau, R., Facciotti, M. T., Pan, M., Glusman, G., Deutsch, E. W., Shannon, P., Chiu, Y., Weng, R.S., Gan, R.R., & Hung, P. (2004). Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Research, 14(11), 2221-2234.

Ballesteros, G. I., Torres-Díaz, C., Bravo, L. A., Balboa, K., Caruso, C., Bertini, L., Proietti, S., & Molina-Montenegro, M. A. (2020). In silico analysis of metatranscriptomic data from the Antarctic vascular plant Colobanthus quitensis: Responses to a global warming scenario through changes in fungal gene expression levels. Fungal Ecology, 43, 100873.

Bayley, S. T., Morton, R. A., & Lanyi, J. K. (1978). Recent developments in the molecular biology of extremely halophilic bacteria. CRC Critical Reviews in Microbiology, 6(2), 151-206.

Bebianno, M. J., & da Fonseca, T. G. (2020). Fate and Effects of Cytostatic Pharmaceuticals in the Marine Environment. In Fate and Effects of Anticancer Drugs in the Environment (pp. 295-330). Springer, Cham.

Becker, E. A., Seitzer, P. M., Tritt, A., Larsen, D., Krusor, M., Yao, A. I., Wu, D., Madern, D., Eisen, J.A., Darling, A.E., & Facciotti, M. T. (2014). Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response. PLoS Genetics, 10(11).

Bei, Q., Moser, G., Wu, X., Müller, C., & Liesack, W. (2019). Metatranscriptomics reveals climate change effects on the rhizosphere microbiomes in European grassland. Soil Biology and Biochemistry, 138, 107604.

Bolhuis, A., Kwan, D., & Thomas, J. R. (2008). Halophilic adaptations of proteins. Protein Adaptation in Extremophiles, 71-104.

Boujelben, I., Yarza, P., Almansa, C., Villamor, J., Maalej, S., Antón, J., and Santos, F. (2012). Virioplankton community structure in Tunisian solar salterns. Applied and Environmental Microbiology, 78(20), 7429-7437.

Bourillot, R., Vennin, E., Dupraz, C., Pace, A., Foubert, A., Rouchy, J. M., Patrier, P., Blanc, P., Bernard, D., Lesseur, J., & Visscher, P. T. (2020). The Record of Environmental and Microbial Signatures in Ancient Microbialites: The Terminal Carbonate Complex from the Neogene Basins of Southeastern Spain. Minerals, 10(3), 276.

Burkhardt, J., Sewald, X., Bauer, B., Saum, S.H., & Müller, V. (2009) Synthesis of glycine betaine from choline in the moderate halophile Halobacillus halophilus: co-regulation of two divergent, polycistronic operons. Environmental Microbiology Reports, 1(1), 38-43.

Bürklen, L., Schöck, F., & Dahl, M. K. (1998). Molecular analysis of the interaction between the Bacillus subtilis trehalose repressor TreR and the tre operator. Molecular and General Genetics MGG, 260(1), 48-55.

Bursy, J., Pierik, A.J., Pica, N., and Bremer, E. (2007) Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase. Journal of Biological Chemistry, 282: 31147–31155

Caruso, C., Rizzo, C., Mangano, S., Poli, A., Di Donato, P., Finore, I., Nicolaus, B., Di Marco, G., Michaud, L., & Giudice, A. L. (2018). Production and biotechnological potential of extracellular polymeric substances from sponge-associated Antarctic bacteria. Applied and Environmental Microbiology, 84(4), e01624-17.

Chen, S., Xu, Y., & Helfant, L. (2020). Geographical Isolation, Buried Depth, and Physicochemical Traits Drive the Variation of Species Diversity and Prokaryotic Community in Three Typical Hypersaline Environments. Microorganisms, 8(1), 120.

Cheng, H. J., Sun, Y. H., Chang, H. W., Cui, F. F., Xue, H. J., Shen, Y. B., Wang, M., & Luo, J. M. (2020). Compatible solutes adaptive alterations in Arthrobacter simplex during exposure to ethanol, and the effect of trehalose on the stress resistance and biotransformation performance. Bioprocess and Biosystems Engineering, 1-14.

DasSarma, S. L., Capes, M. D., DasSarma, P., & DasSarma, S. (2010). HaloWeb: the haloarchaeal genomes database. Saline Systems, 6(1), 12.

DasSarma, S., & DasSarma, P. (2015). Halophiles and their enzymes: negativity put to good use. Current Opinion in Microbiology, 25, 120-126.

De Vitis, Valerio, Benedetta Guidi, Martina Letizia Contente, Tiziana Granato, Paola Conti, Francesco Molinari, Elena Crotti et al. "Marine microorganisms as source of stereoselective esterases and ketoreductases: kinetic resolution of a prostaglandin intermediate." Marine Biotechnology 17, no. 2 (2015): 144-152.

Decho, A. W., & Gutierrez, T. (2017). Microbial extracellular polymeric substances (EPSs) in ocean systems. Frontiers in Microbiology, 8, 922.

Deng, Y., Ruan, Y., Ma, B., Timmons, M. B., Lu, H., Xu, X., Zhao, H., & Yin, X. (2019). Multi-omics analysis reveals niche and fitness differences in typical denitrification microbial aggregations. Environment International, 132, 105085.

Diken, E., Ozer, T., Arikan, M., Emrence, Z., Oner, E. T., Ustek, D., & Arga, K. Y. (2015). Genomic analysis reveals the biotechnological and industrial potential of levan producing halophilic extremophile, Halomonas smyrnensis AAD6T. SpringerPlus, 4(1), 393.

Dillon, J. G., Carlin, M., Gutierrez, A., Nguyen, V., & McLain, N. (2013). Patterns of microbial diversity along a salinity gradient in the Guerrero Negro solar saltern, Baja CA Sur, Mexico. Frontiers in Microbiology, 4, 399.

Duru, I. C., Laine, P., Andreevskaya, M., Paulin, L., Kananen, S., Tynkkynen, S., Auvinen, P., & Smolander, O. P. (2018). Metagenomic and metatranscriptomic analysis of the microbial community in Swiss-type Maasdam cheese during ripening. International Journal of Food Microbiology, 281, 10-22.

Falk, N., Reid, T., Skoyles, A., Grgicak-Mannion, A., Drouillard, K., & Weisener, C. G. (2019). Microbial metatranscriptomic investigations across contaminant gradients of the Detroit River. Science of the Total Environment, 690, 121-131.

Fernández, A. B., Ghai, R., Martin-Cuadrado, A. B., Sanchez-Porro, C., Rodriguez-Valera, F., and Ventosa, A. (2014). Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiology Ecology, 88(3), 623-635.

Fernández, A. B., León, M. J., Vera, B., Sánchez-Porro, C., and Ventosa, A. (2014). Metagenomic sequence of prokaryotic microbiota from an intermediate-salinity pond of a saltern in Isla Cristina, Spain. Genome announcements, 2(1), e00045-14.doi: 10.1128/genomeA.00045-14.

Fernández, A. B., Vera-Gargallo, B., Sánchez-Porro, C., Ghai, R., Papke, R. T., Rodriguez-Valera, F., & Ventosa, A. (2014). Comparison of prokaryotic community structure from Mediterranean and Atlantic saltern concentrator ponds by a metagenomic approach. Frontiers in Microbiology, 5, 196.

Fierer, N., Leff, J. W., Adams, B. J., Nielsen, U. N., Bates, S. T., Lauber, C. L., Owens S, Gilbert J.A, Wall D.H and Caporaso, J. G. (2012). Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences, 109(52), 21390-21395. http://dx.doi.org/10.1073/ pnas.1215210110.

Forster, D., Behnke, A., & Stoeck, T. (2012). Meta-analyses of environmental sequence data identify anoxia and salinity as parameters shaping ciliate communities. Systematics and Biodiversity, 10(3), 277-288.

Fujita, M. J., Kimura, N., Sakai, A., Ichikawa, Y., Hanyu, T., & Otsuka, M. (2011). Cloning and heterologous expression of the vibrioferrin biosynthetic gene cluster from a marine metagenomic library. Bioscience, Biotechnology, and Biochemistry, 75(12), 2283-2287.

Fujita, M. J., Kimura, N., Yokose, H., & Otsuka, M. (2012). Heterologous production of bisucaberin using a biosynthetic gene cluster cloned from a deep sea metagenome. Molecular BioSystems, 8(2), 482-485.

Galinski, E. A., & Trüper, H. G. (1994). Microbial behaviour in salt-stressed ecosystems. FEMS Microbiology Reviews, 15(2-3), 95-108.

Ghai, R., Pašić, L., Fernández, A. B., Martin-Cuadrado, A. B., Mizuno, C. M., McMahon, K. D., Papke R.T, Stepanauskas R, Rodriguez-Brito B, Rohwer F and Sánchez-Porro, C. (2011). New abundant microbial groups in aquatic hypersaline environments. Scientific Reports, 1, 135.

Giovanella, P., Vieira, G. A., Otero, I. V. R., Pellizzer, E. P., de Jesus Fontes, B., & Sette, L. D. (2020). Metal and organic pollutants bioremediation by extremophile microorganisms. Journal of Hazardous Materials, 382, 121024.

Górecki, K., Hägerhäll, C., & Drakenberg, T. (2014). The Na+ transport in gram-positive bacteria defect in the Mrp antiporter complex measured with 23Na nuclear magnetic resonance. Analytical Biochemistry, 445, 80-86.

Gunde-Cimerman, N., Plemenitaš, A., & Oren, A. (2018). Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiology Reviews, 42(3), 353-375.

Gupta, S. K., Rai, A. K., Sarim, K. M., Sharma, A., Budhlakoti, N., Arora, D., Verma, D.K., & Singh, D. P. (2019). Metaproteomic data of maize rhizosphere for deciphering functional diversity. Data in Brief, 27, 104574.

Gutierrez, T., Morris, G., Ellis, D., Mulloy, B., & Aitken, M. D. (2020). Production and characterisation of a marine Halomonas surface-active exopolymer. Applied Microbiology and Biotechnology, 104(3), 1063-1076.

Hasan, H., Gul, A., Amir, R., Ali, M., Kubra, G., Yousaf, S., Ajmal, K.B., Naseer, H., & Keyani, R. (2020). Role of osmoprotectants and drought tolerance in wheat. In Climate Change and Food Security with Emphasis on Wheat (pp. 207-216). Academic Press.

Hernández-Jarguín, A., Díaz-Sánchez, S., Villar, M., & de la Fuente, J. (2018). Integrated metatranscriptomics and metaproteomics for the characterization of bacterial microbiota in unfed Ixodes ricinus. Ticks and Tick-borne Diseases, 9(5), 1241-1251.

Hoffmann, T., & Bremer, E. (2017). Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biological chemistry, 398(2), 193-214.

Huan, R., Huang, J., Liu, D., Wang, M., Liu, C., Zhang, Y., Yi, C., Xiao, D., & He, H. (2019). Genome sequencing of Mesonia algae K4-1 reveals its adaptation to the Arctic ocean. Frontiers in Microbiology, 10, 2812.

Inbar, L., and Lapidot, A. (1988) The structure and biosynthesis of new tetrahydropyrimidine derivatives in actinomycin D producer Streptomyces parvulus. Use of 13C- and 15N-labeled L-glutamate and 13C and 15N NMR spectroscopy. Journal of Biological Chemistry, 263: 16014–16022.

Jacob, J. H., Hussein, E. I., Shakhatreh, M. A. K., and Cornelison, C. T. (2017). Microbial community analysis of the hypersaline water of the Dead Sea using high‐throughput amplicon sequencing. MicrobiologyOpen, 6(5), e00500.

Jebbar, M., Hickman-Lewis, K., Cavalazzi, B., Taubner, R. S., Simon, K. M. R., & Antunes, A. (2020). Microbial Diversity and Biosignatures: An Icy Moons Perspective. Space Science Reviews, 216(1), 10.

Jin, M., Gai, Y., Guo, X., Hou, Y., & Zeng, R. (2019). Properties and applications of extremozymes from deep-sea extremophilic microorganisms: A mini review. Marine drugs, 17(12), 656.

John, J., Siva, V., Richa, K., Arya, A., & Kumar, A. (2019). Life in High Salt Concentrations with Changing Environmental Conditions: Insights from Genomic and Phenotypic Analysis of Salinivibrio sp. Microorganisms, 7(11), 577.

Kalogerakis, N., Arff, J., Banat, I. M., Broch, O. J., Daffonchio, D., Edvardsen, T., Eguiraun, H., Giuliano, L., Handå, A., López-de-Ipiña, K., & Marigomez, I. (2015). The role of environmental biotechnology in exploring, exploiting, monitoring, preserving, protecting and decontaminating the marine environment. New Biotechnology, 32(1), 157-167.

Kappes, R. M., Kempf, B., Kneip, S., Boch, J., Gade, J., Meier‐Wagner, J., & Bremer, E. (1999). Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis. Molecular Microbiology, 32(1), 203-216.

Kimura, Y., Kawasaki, S., Yoshimoto, H., & Takegawa, K. (2010). Glycine betaine biosynthesized from glycine provides an osmolyte for cell growth and spore germination during osmotic stress in Myxococcus xanthus. Journal of bacteriology, 192(5), 1467-1470.

Kixmüller, D., & Greie, J. C. (2012). An ATP‐driven potassium pump promotes long‐term survival of Halobacterium salinarum within salt crystals. Environmental Microbiology Reports, 4(2), 234-241.

Kolman, M. A., Nishi, C. N., Perez-Cenci, M., & Salerno, G. L. (2015). Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation. Life, 5(1), 102-126.

Kosar, F., Akram, N. A., Sadiq, M., Al-Qurainy, F., & Ashraf, M. (2019). Trehalose: a key organic osmolyte effectively involved in plant abiotic stress tolerance. Journal of Plant Growth Regulation, 38(2), 606-618.

La Cono, V., Smedile, F., Bortoluzzi, G., Arcadi, E., Maimone, G., Messina, E., Borghini M, Oliveri E, Mazzola S, L'Haridon S, and Toffin, L. (2011). Unveiling microbial life in new deep‐sea hypersaline Lake Thetis. Part I: Prokaryotes and environmental settings. Environmental Microbiology, 13(8), 2250-2268.

Lanyi, J. K. (1974). Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriological reviews, 38(3), 272.

Leon, M. J., Ghai, R., Fernandez, A. B., Sanchez-Porro, C., Rodriguez-Valera, F., & Ventosa, A. (2013). Draft genome of Spiribacter salinus M19-40, an abundant gammaproteobacterium in aquatic hypersaline environments. Genome Announcement., 1(1), e00179-12.

León, M. J., Hoffmann, T., Sánchez-Porro, C., Heider, J., Ventosa, A., & Bremer, E. (2018). Compatible solute synthesis and import by the moderate halophile Spiribacter salinus: Physiology and genomics. Frontiers in Microbiology, 9, 108.

Li, F., Neves, A. L., & Ghoshal, B. (2018). Symposium review: mining metagenomic and metatranscriptomic data for clues about microbial metabolic functions in ruminants. Journal of dairy science, 101(6), 5605-5618.

Li, W., Zhuang, J. L., Zhou, Y. Y., Meng, F. G., Kang, D., Zheng, P., & Shapleigh, J. P. (2020). Metagenomics reveals microbial community differences lead to differential nitrate production in anammox reactors with differing nitrogen loading rates. Water Research, 169, 115279.

Li, X., Zhu, Y. G., Shaban, B., Bruxner, T. J., Bond, P. L., & Huang, L. (2015). Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length copA genes. Scientific Reports, 5, 13258.

Lin, Y. W., Tuan, N. N., & Huang, S. L. (2016). Metaproteomic analysis of the microbial community present in a thermophilic swine manure digester to allow functional characterization: a case study. International Biodeterioration & Biodegradation, 115, 64-73.

Litalien, A., & Zeeb, B. (2020). Curing the earth: A review of anthropogenic soil salinization and plant-based strategies for sustainable mitigation. Science of The Total Environment, 698, 134235.

López‐López, A., Yarza, P., Richter, M., Suárez‐Suárez, A., Antón, J., Niemann, H., and Rosselló‐Móra, R. (2010). Extremely halophilic microbial communities in anaerobic sediments from a solar saltern. Environmental Microbiology Reports, 2(2), 258-271.

López-Pérez, M., Ghai, R., Leon, M. J., Rodríguez-Olmos, Á., Copa-Patiño, J. L., Soliveri, J., Sanchez-Porro, C., Ventosa, A., & Rodriguez-Valera, F. (2013). Genomes of “Spiribacter”, a streamlined, successful halophilic bacterium. BMC Genomics, 14(1), 787.

Lou, J., Liu, M., Gu, J., Liu, Q., Zhao, L., Ma, Y., & Wei, D. (2019). Metagenomic sequencing reveals microbial gene catalogue of phosphinothricin-utilized soils in South China. Gene, 711, 143942.

Lozupone, C. A., & Knight, R. (2007). Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences, 104(27), 11436-11440.

Ma, L., Wang, H., Wu, J., Wang, Y., Zhang, D., & Liu, X. (2019). Metatranscriptomics reveals microbial adaptation and resistance to extreme environment coupling with bioleaching performance. Bioresource technology, 280, 9-17.

Mapelli, F., Crotti, E., Molinari, F., Daffonchio, D., & Borin, S. (2016). Extreme marine environments (brines, seeps, and smokers). In The Marine Microbiome (pp. 251-282). Springer, Cham.

Martínez-Espinosa, R. M. (2020). Heterologous and Homologous Expression of Proteins from Haloarchaea: Denitrification as Case of Study. International Journal of Molecular Sciences, 21(1), 82.

Martínez-Espinosa, R. M. (2020). Heterologous and Homologous Expression of Proteins from Haloarchaea: Denitrification as Case of Study. International Journal of Molecular Sciences, 21(1), 82.

Maturrano, L., Santos, F., Rosselló-Mora, R., and Antón, J. (2006). Microbial diversity in Maras salterns, a hypersaline environment in the Peruvian Andes. Applied and Environmental Microbiology, 72(6), 3887-3895

Mavromatis, K., Ivanova, N., Anderson, I., Lykidis, A., Hooper, S. D., Sun, H., Kunin, V., Lapidus, A., Hugenholtz, P., Patel, B., & Kyrpides, N. C. (2009). Genome analysis of the anaerobic thermohalophilic bacterium Halothermothrix orenii. PLoS One, 4(1).

McGenity, T. J., & Oren, A. (2012). Hypersaline environments. Life at extremes: environments, organisms and strategies for survival, 402-437.

Mevarech, M., Frolow, F., & Gloss, L. M. (2000). Halophilic enzymes: proteins with a grain of salt. Biophysical Chemistry, 86(2-3), 155-164.

Mitchell, W. J. (2015). The phosphotransferase system in solventogenic clostridia. Journal of Molecular Microbiology and Biotechnology, 25(2-3), 129-142.

Mitchell, W. J. (2016). Sugar uptake by the solventogenic clostridia. World Journal of Microbiology and Biotechnology, 32(2), 32.

Mongodin, E. F., Nelson, K. E., Daugherty, S., Deboy, R. T., Wister, J., Khouri, H., Weidman, J., Walsh, D.A., Papke, R.T., Perez, G.S., & Sharma, A. K. (2005). The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proceedings of the National Academy of Sciences, 102(50), 18147-18152.

Müller, V., and Oren, A. (2003). Metabolism of chloride in halophilic prokaryotes. Extremophiles, 7(4), 261-266.

Nayfach, S., & Pollard, K. S. (2016). Toward accurate and quantitative comparative metagenomics. Cell, 166(5), 1103-1116.

Niero, M., Righetto, I., Beneventi, E., Polverino de Laureto, P., Fraaije, M. W., Filippini, F., & Bergantino, E. (2020). Unique Features of a New Baeyer–Villiger Monooxygenase from a Halophilic Archaeon. Catalysts, 10(1), 128.

Nyyssölä, A., Kerovuo, J., Kaukinen, P., von Weymarn, N., and Reinikainen, T. (2000). Extreme halophiles synthesize betaine from glycine by methylation. Journal of Biological Chemistry, 275(29), 22196-22201.

Oberbeckmann, S., & Labrenz, M. (2020). Marine microbial assemblages on microplastics: Diversity, adaptation, and role in degradation. Annual Revierws,

Ohtani, K., & Shimizu, T. (2015). Regulation of toxin gene expression in Clostridium perfringens. Research in microbiology, 166(4), 280-289.

Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Sal Syst. 2008; 4: 13

Oren, A. (1999). Bioenergetic aspects of halophilism. Microbiological and Molecular Biology Reviews, 63(2), 334-348.

Oren, A. (2006). Life at high salt concentrations. The Prokaryotes, 3, 263-282.

Oren, A., Heldal, M., Norland, S., & Galinski, E. A. (2002). Intracellular ion and organic solute concentrations of the extremely halophilic bacterium Salinibacter ruber. Extremophiles, 6(6), 491-498.

Oren, A., Larimer, F., Richardson, P., Lapidus, A., & Csonka, L. N. (2005). How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles, 9(4), 275-279.

Oyewusi, H. A., Wahab, R. A., & Huyop, F. (2020). Dehalogenase-producing halophiles and their potential role in bioremediation. Marine Pollution Bulletin, 160, 111603.

Pachiadaki, M. G., Yakimov, M. M., LaCono, V., Leadbetter, E., & Edgcomb, V. (2014). Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin. The ISME Journal, 8(12), 2478-2489.

Park, M., Mitchell, W. J., & Rafii, F. (2016). Effect of trehalose and trehalose transport on the tolerance of Clostridium perfringens to environmental stress in a wild type strain and its fluoroquinolone-resistant mutant. International Journal of Microbiology, 2016.

Pérez-Llano, Y., Rodríguez-Pupo, E. C., Druzhinina, I. S., Chenthamara, K., Cai, F., Gunde-Cimerman, N., Zalar, P., Gostinčar, C., Kostanjšek, R., Folch-Mallol, J.L., & Batista-García, R. A. (2020). Stress Reshapes the Physiological Response of Halophile Fungi to Salinity. Cells, 9(3), 525.

Petrovicˇ, U., Gunde‐Cimerman, N., & Plemenitasˇ, A. (2002). Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Molecular Microbiology, 45(3), 665-672.

Podell, S., Ugalde, J. A., Narasingarao, P., Banfield, J. F., Heidelberg, K. B., & Allen, E. E. (2013). Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One, 8(4), e61692.

Prakash, J., & Chandra, P. (2020). Halophilic Microbes from Plant Growing Under the Hypersaline Habitats and Their Application for Plant Growth and Mitigation of Salt Stress. In Plant Microbiomes for Sustainable Agriculture (pp. 317-349). Springer, Cham.

Purvis, J. E., Yomano, L. P., & Ingram, L. O. (2005). Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Applied and Environmental Microbiology, 71(7), 3761-3769.

Raddadi, N., Cherif, A., Daffonchio, D., Neifar, M., and Fava, F. (2015). Biotechnological applications of extremophiles, extremozymes and extremolytes. Applied. Microbiology Biotechnology, 99, 7907–7913. doi: 10.1007/ s00253-015-6874-9

Raddadi, N., Giacomucci, L., Marasco, R., Daffonchio, D., Cherif, A., and Fava, F. (2018).Bacterial poly extremotolerant bioemulsifiers from arid soils improve water retention capacity and humidity uptake in sandy soil. Microb. Cell. Fact. 17:83.doi:10.1186/s12934-018-0934-7

Robbins, R. J., Krishtalka, L., & Wooley, J. C. (2016). Advances in biodiversity: metagenomics and the unveiling of biological dark matter. Standards in Genomic Sciences, 11(1), 69.

Roeßler, M., & Müller, V. (2001). Chloride dependence of glycine betaine transport in Halobacillus halophilus. FEBS letters, 489(2-3), 125-128.

Roeβler, M., and Müller, V. (2002). Chloride, a new environmental signal molecule involved in gene regulation in a moderately halophilic bacterium, Halobacillus halophilus. Journal of Bacteriology, 184(22), 6207-6215

Ruvindy, R., White III, R. A., Neilan, B. A., and Burns, B. P. (2016). Unravelling core microbial metabolisms in the hypersaline microbial mats of Shark Bay using high-throughput metagenomics. The ISME journal, 10(1), 183.

Sanderson, J. (Ed.). (2020). Landscape ecology: a top down approach. CRC Press.

Sarsaiya, S., Jain, A., Jia, Q., Fan, X., Shu, F., Chen, Z., Zhou, Q., Shi, J., & Chen, J. (2020). Molecular Identification of Endophytic Fungi and Their Pathogenicity Evaluation Against Dendrobium nobile and Dendrobium officinale. International Journal of Molecular Sciences, 21(1), 316.

Saum, R., Mingote, A., Santos, H., and Müller, V. (2009) A novel limb in the osmoregulatory network of Methanosarcina mazei Gö1: Ne -acetyl-b-lysine can be substituted by glutamate and alanine. Environ Microbiol 11: 1056–1065.

Saum, S. H. & Müller, V. (2008). Regulation of osmoadaptation in the moderate halophile Halobacillus halophilus: chloride, glutamate and switching osmolyte strategies. Saline Systems. 4(4), 2014.

Saum, S. H., Pfeiffer, F., Palm, P., Rampp, M., Schuster, S. C., Müller, V., and Oesterhelt, D. (2013). Chloride and organic osmolytes: a hybrid strategy to cope with elevated salinities by the moderately halophilic, chloride‐dependent bacterium Halobacillus halophilus. Environmental Microbiology, 15(5), 1619-1633.

Saum, S. H., Roeßler, M., Koller, C., Sydow, J. F., and Müller, V. (2007). Glutamate restores growth but not motility in the absence of chloride in the moderate halophile Halobacillus halophilus. Extremophiles, 11(5), 711-717.

Saum, S. H., Sydow, J. F., Palm, P., Pfeiffer, F., Oesterhelt, D. and Müller, V. (2006). Biochemical and molecular characterization of the biosynthesis of glutamine and glutamate, two major compatible solutes in the moderately halophilic bacterium Halobacillus halophilus. Journal of Bacteriology. 188(19), 6808-6815.

Saum, S.H., and Müller, V. (2007) Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus. Journal of bacteriology,189: 6968–6975.

Saum, S.H., and Müller, V. (2008) Growth phase-dependent switch in osmolyte strategy in a moderate halophile: ectoine is a minor osmolyte but major stationary phase solute in Halobacillus halophilus. Environmental Microbiology 10: 716–726.

Saum, S.H., Sydow, J.F., Palm, P., Pfeiffer, F., Oesterhelt, D., and Müller, V. (2006) Biochemical and molecular charac1632 S. H. Saum et al. © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 15, 1619–1633 terization of the biosynthesis of glutamine and glutamate, two major compatible solutes in the moderately halophilic bacterium Halobacillus halophilus. J Bacteriol 188: 6808– 6815.

Schloss, P. D., & Handelsman, J. (2005). Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biology, 6(8), 229.

Schmid, A. K., Allers, T., & DiRuggiero, J. (2020). SnapShot: Microbial Extremophiles. Cell, 180(4), 818-818.

Sharma, A. K., Kikani, B. A., & Singh, S. P. (2020). Biochemical, thermodynamic and structural characteristics of a biotechnologically compatible alkaline protease from a haloalkaliphilic, Nocardiopsis dassonvillei OK-18. International Journal of Biological Macromolecules.

Silva, C., Martins, M., Jing, S., Fu, J., & Cavaco-Paulo, A. (2018). Practical insights on enzyme stabilization. Critical Reviews in Biotechnology, 38(3), 335-350.

Strom, A. R., & Kaasen, I. (1993). Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Molecular Microbiology, 8(2), 205-210.

Styrvold, O. B., Falkenberg, P., Landfald, B., Eshoo, M. W., Bjørnsen, T., & Strøm, A. R. (1986). Selection, mapping, and characterization of osmoregulatory mutants of Escherichia coli blocked in the choline-glycine betaine pathway. Journal of Bacteriology, 165(3), 856-863.

Tang, K. (2020). Chemical Diversity and Biochemical Transformation of Biogenic Organic Sulfur in the Ocean. Frontiers in Marine Science, 7, 68.

Tringe, S. G., Von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., Chang, H. W., Podar, M., Short, J.M., Mathur, E.J., Detter, J.C., & Bork, P. (2005). Comparative metagenomics of microbial communities. Science, 308(5721), 554-557.

Vargas, C., Jebbar, M., Carrasco, R., Blanco, C., Calderón, M. I., Iglesias‐Guerra, F., & Nieto, J. J. (2006). Ectoines as compatible solutes and carbon and energy sources for the halophilic bacterium Chromohalobacter salexigens. Journal of Applied Microbiology, 100(1), 98-107.

Varshney, P., Mikulic, P., Vonshak, A., Beardall, J., & Wangikar, P. P. (2015). Extremophilic micro-algae and their potential contribution in biotechnology. Bioresource technology, 184, 363-372.

Vavourakis, C. D., Ghai, R., Rodriguez-Valera, F., Sorokin, D. Y., Tringe, S. G., Hugenholtz, P., and Muyzer, G. (2016). Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Frontiers in Microbiology, 7, 211.

Ventosa, A., Nieto, J. J., and Oren, A. (1998). Biology of moderately halophilic aerobic bacteria. Microbiology and Molecular Biology Reviews, 62(2), 504-544

Vera-Gargallo, B., and Ventosa, A. (2018). Metagenomic Insights into the Phylogenetic and Metabolic Diversity of the Prokaryotic Community Dwelling in Hypersaline Soils from the Odiel Saltmarshes (SW Spain). Genes, 9(3), 152.

Waditee, R., Bhuiyan, M. N. H., Rai, V., Aoki, K., Tanaka, Y., Hibino, T., Suzuki S, Takano J, Jagendorf AT, Takabe T, and Takabe, T. (2005). Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proceedings of the National Academy of Sciences, 102(5), 1318-1323.

Wang, H. L., & Sun, L. (2017). Comparative metagenomics reveals insights into the deep-sea adaptation mechanism of the microorganisms in Iheya hydrothermal fields. World Journal of Microbiology and Biotechnology, 33(5), 86.

Weinisch, L., Kirchner, I., Grimm, M., Kühner, S., Pierik, A. J., Rosselló-Móra, R., & Filker, S. (2019). Glycine betaine and ectoine are the major compatible solutes used by four different halophilic heterotrophic ciliates. Microbial Ecology, 77(2), 317-331.

Weinisch, L., Kühner, S., Roth, R., Grimm, M., Roth, T., Netz, D. J., ... & Filker, S. (2018). Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum. PLoS biology, 16(1), e2003892.

Wood, J. M., Bremer, E., Csonka, L. N., Kraemer, R., Poolman, B., van der Heide, T., & Smith, L. T. (2001). Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 130(3), 437-460.

Yakimov, M. M., La Cono, V., Spada, G. L., Bortoluzzi, G., Messina, E., Smedile, F., Arcadi E, Borghini M, Ferrer M, Schmitt‐Kopplin P, and Hertkorn, N. (2015). Microbial community of the deep‐sea brine Lake Kryos seawater–brine interface is active below the chaotropicity limit of life as revealed by recovery of mRNA. Environmental Microbiology, 17(2), 364-382.

Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology, 208(15), 2819-2830.

Yang, H. W., Song, J. Y., Cho, S. M., Kwon, H. C., Pan, C. H., & Park, Y. I. (2020). Genomic Survey of Salt Acclimation-Related Genes in the Halophilic Cyanobacterium Euhalothece sp. Z-M001. Scientific Reports, 10.

Yau, S., Lauro, F. M., Williams, T. J., DeMaere, M. Z., Brown, M. V., Rich, J., Gibson J.A and Cavicchioli, R. (2013). Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake. The ISME Journal, 7(10), 1944.

Zeaiter, Z., Marasco, R., Booth, J. M., Prosdocimi, E. M., Mapelli, F., Callegari, M., Fusi, M., Michoud, G., Molinari, F., Daffonchio, D., & Borin, S. (2019). Phenomics and genomics reveal adaptation of Virgibacillus dokdonensis strain 21D to its origin of isolation, the seawater-brine interface of the Mediterranean Sea deep hypersaline anoxic basin Discovery. Frontiers in Microbiology, 10, 1304.




DOI: http://dx.doi.org/10.11594/jtls.11.03.11

Copyright (c) 2021 Habeebat Adekilekun Oyewusi, Fahrul Huyop, Roswanira Abdul Wahab