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A Blue-Purple Pigment-Producing Bacterium Isolated from the Vezelka River in the City of Belgorod

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A Blue-Purple Pigment-Producing Bacterium Isolated from the Vezelka River in the City of Belgorod microorganisms Article A Blue-Purple Pigment-Producing Bacterium Isolated from the Vezelka River in the City of Belgorod Nikita S. Lyakhovchenko 1, Tatiana N. Abashina 2, Valentina N. Polivtseva 2 , Vladislav Yu. Senchenkov 1, Daniil A. Pribylov 1, Anna A. Chepurina 1, Ilja A. Nikishin 1, Alina A. Avakova 1, Michael A. Goyanov 1, Elizaveta D. Gubina 1, Daria A. Churikova 1, Alexander A. Sirotin 1, Nataliya E. Suzina 2 and Inna P. Solyanikova 1,2,* 1 Federal State Autonomous Educational Institution of Higher Education, Belgorod National Research University, 308015 Belgorod, Russia; [email protected] (N.S.L.); [email protected] (V.Y.S.); [email protected] (D.A.P.); [email protected] (A.A.C.); [email protected] (I.A.N.); [email protected] (A.A.A.);[email protected] (M.A.G.); [email protected] (E.D.G.); [email protected] (D.A.C.); [email protected] (A.A.S.) 2 G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Center for Biological Research of the Russian Academy of Sciences, Pushchino, 142290 Moscow, Russia; [email protected] (T.N.A.); [email protected] (V.N.P.); [email protected] (N.E.S.) * Correspondence: [email protected] Abstract: Violacein is a biotechnologically significant secondary metabolite due to its antibacterial, antifungal, and other properties. Isolation, research, and identification of violacein producing strains are of interest for the development of biotechnological processes, in order to enhance the biosynthesis of this compound. The purpose of the present work was to study the properties of a newly isolated bacterium capable of synthesizing blue-purple pigment. An aboriginal bacterium Citation: Lyakhovchenko, N.S.; was isolated from the coastal zone of the Vezelka River in the city of Belgorod. Based on chemical Abashina, T.N.; Polivtseva, V.N.; and spectrophotometric studies of the crude ethanol extract, the pigment was identified as violacein, Senchenkov, V.Y.; Pribylov, D.A.; and the isolate was assigned to the group of violacein-forming bacteria, which includes bacteria Chepurina, A.A.; Nikishin, I.A.; of the genera Chromobacterium, Iodobacter, Janthinobacterium, Duganella, Collimonas, and Massilia. Avakova, A.A.; Goyanov, M.A.; Based on cultural, morphological, tinctorial, physiological, and biochemical properties, as well Gubina, E.D.; et al. A Blue-Purple as analysis of the 16S rRNA gene sequence, the new isolated strain was assigned to the genus Pigment-Producing Bacterium Janthinobacterium. The isolated strain is capable of suppressing the growth of a number of fungal Isolated from the Vezelka River in the and bacterial phytopathogens. For representatives of the genus Janthinobacterium, their inhibitory City of Belgorod. Microorganisms 2021, influence on cyanobacteria was shown for the first time. 9, 102. https://doi.org/10.3390/ microorganisms9010102 Keywords: Janthinobacterium sp., identification; violacein; biotechnological significance Received: 26 November 2020 Accepted: 30 December 2020 Published: 5 January 2021 1. Introduction Publisher’s Note: MDPI stays neu- Bacterial cells produce a huge number of biologically active compounds, including tral with regard to jurisdictional clai- vitamins, amino acids, antibiotics, and enzymes [1]. At present, the biotechnological ms in published maps and institutio- significance of one more group of secondary metabolites of bacteria, pigments, has been nal affiliations. estimated [2]. The ability to synthesize pigments that differ in chemical composition, color, and solubility is characteristic of many microorganisms [3]. The role of pigments for microorganisms may be to participate in respiration processes, to protect against ultraviolet radiation. In addition, some microorganisms synthesize pig- Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. ments that have antibacterial and/or antifungal properties. The formation of secondary This article is an open access article metabolites by microorganisms, providing their antagonistic effects, is an adaptation to the distributed under the terms and con- conditions of existence in the microbial community along with other forms of interaction ditions of the Creative Commons At- both within the consortium and for other systems associated with it. The phenomenon tribution (CC BY) license (https:// of antagonism among microorganisms is widely used in medicine and agriculture. Live creativecommons.org/licenses/by/ antagonist microbes are used in medical practice to combat dysbacteriosis and candidomy- 4.0/). cosis, which sometimes occur with the use of broad-spectrum antibiotics, for therapy and Microorganisms 2021, 9, 102. https://doi.org/10.3390/microorganisms9010102 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 18 ondary metabolites by microorganisms, providing their antagonistic effects, is an adapta- tion to the conditions of existence in the microbial community along with other forms of interaction both within the consortium and for other systems associated with it. The phe- nomenon of antagonism among microorganisms is widely used in medicine and agricul- Microorganisms 2021, 9, 102 2 of 19 ture. Live antagonist microbes are used in medical practice to combat dysbacteriosis and candidomycosis, which sometimes occur with the use of broad-spectrum antibiotics, for therapy and prevention of various infectious diseases. Antagonism between microorgan- preventionisms attracts of the various attention infectious of scientists diseases. and Antagonism agricultural between workers microorganisms for its use in the attracts fight theagainst attention phytopathogenic of scientists organisms and agricultural that cause workers considerable for its use harm in to the agricultural fight against produc- phy- topathogeniction [4]. Thus, organisms bacteria that of cause the considerablegenera Chromobacterium harm to agricultural, Iodobacter production, Janthobacterium [4]. Thus,, bacteriaDuganella of, theCollimonas genera, Chromobacteriumand Massilia are ,ableIodobacter to form, Janthobacterium a purple pigment-violacein, Duganella, Collimonas or (3- (1,2-, anddihydro-Massilia (5-hydroxy-1H-indol-3-yl)are able to form a purple pigment-violacein-2-oxo-3H-pyrrol-3-ylidene) or (3- (1,2-dihydro- -1,3-dihydro-2H-indol- (5-hydroxy-1H- indol-3-yl)2-one) (Figure -2-oxo-3H-pyrrol-3-ylidene) 1A), which has important -1,3-dihydro-2H-indol-2-one) biological activity (antitumor, (Figure antiviral,1A), antibac- which hasterial, important antifungal, biological antiprotozoal, activity (antitumor,and antiparasitic antiviral, activity) antibacterial, and significant antifungal, pharmacologi- antiproto- zoal,cal potential and antiparasitic [5]. activity) and significant pharmacological potential [5]. FigureFigure 1.1. TheThe structurestructure ofof thethe violaceinviolacein ((AA),), deoxyviolaceindeoxyviolacein ( B(B),), and and oxyviolacein oxyviolacein ( C(C)) molecules molecules [ 6[6].]. ItIt isis known known that that the the formation formation of of violacein violacein is due is due to the to mechanismsthe mechanisms of the of sense the sense of quo- of rum.quorum. Based Based on the on fact the thatfact thethat pigment the pigment is visible is visible to the to naked the naked eye, violacein-synthesizing eye, violacein-synthe- bacteriasizing bacteria act as aact convenient as a convenient model model in studies in studies of the of effect the effect of various of various molecules molecules on the on sensethe sense of quorum. of quorum. The violaceinThe violacein biosynthetic biosynthet pathwayic pathway involves involves five genes, five genes, namely namelyvioA, vioBvioA,,vioC vioB,,vioD vioC,, andvioDvioE, and, identified vioE, identified in bacteria in bacteria by the by condensation the condensation of two of L-tryptophan two L-tryp- moleculestophan molecules [6]. [6]. ByBy thethe creationcreation ofof aa compositioncomposition of violacein and an antagonist BdellovibrioBdellovibrio bacterio- bacteri- ovorusvorus HD100,HD100, active active against a polymicrobialpolymicrobial system consistingconsisting ofof StaphylococcusStaphylococcus aureusaureus,, AcinetobacterAcinetobacter baumanniibaumannii,, Bacillus cereus ,, and and KlebsiellaKlebsiella pneumoniae pneumoniae, ,it it was was shown shown that that viola- vio- laceincein can can be be used used in in complex complex systems to controlcontrol undesiredundesired microflora.microflora. TheThe antagonisticantagonistic efficacyefficacy ofof violaceinviolacein andand B.B. bacteriovorusbacteriovorus HD100HD100 waswas 19%19% andand 68%,68%, respectively,respectively,whereas whereas thethe jointjoint activityactivity waswas 99.98%.99.98%. AtAt thethe samesame time,time, violaceinviolacein hadhad nono effecteffect ononB. B. bacteriovorusbacteriovorus HD100HD100 [[7].7]. BasedBased onon the the literature literature data, data, violacein violacein (0.9 µ(0.9M) hadμM) ahad stimulating a stimulating effect on effect the produc- on the tivityproductivity of recombinant of recombinant immunoglobulin immunoglobulin by Chinese by hamster Chinese ovary hamster cells ovary by 37.6%. cells Theby 37.6%. study ofThe the study authors of the reveals authors another reveals biotechnological another biotec significancehnological significance of the pigment, of the in additionpigment, toin theaddition antagonistic to the propertiesantagonistic described properties earlier, descri sobed violacein earlier, can so be violacein used as acan stimulant
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