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Bacterial and Protozoan Lipoxygenases Could Be Involved in Cell-To-Cell Signaling and Immune Response Suppression

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Bacterial and Protozoan Lipoxygenases Could Be Involved in Cell-To-Cell Signaling and Immune Response Suppression ISSN 0006-2979, Biochemistry (Moscow), 2020, Vol. 85, No. 9, pp. 1048-1063. © Pleiades Publishing, Ltd., 2020. Russian Text © The Author(s), 2020, published in Biokhimiya, 2020, Vol. 85, No. 9, pp. 1256-1273. Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM20-168, September 3, 2020. Bacterial and Protozoan Lipoxygenases Could be Involved in Cell-to-Cell Signaling and Immune Response Suppression G. F. Kurakin1,a*, A. M. Samoukina2, and N. A. Potapova3,4 1Department of Biochemistry and Laboratory Medicine, Tver State Medical University, Ministry of Health of the Russian Federation, 170100 Tver, Russia 2Department of Microbiology, Virology, and Immunology, Tver State Medical University, Ministry of Health of the Russian Federation, 170100 Tver, Russia 3Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, 127051 Moscow, Russia 4Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119234 Moscow, Russia ae-mail: [email protected] Received June 19, 2020 Revised June 22, 2020 Accepted June 22, 2020 Abstract—Lipoxygenases are found in animals, plants, and fungi, where they are involved in a wide range of cell-to-cell sig- naling processes. The presence of lipoxygenases in a number of bacteria and protozoa has been also established, but their biological significance remains poorly understood. Several hypothetical functions of lipoxygenases in bacteria and protozoa have been suggested without experimental validation. The objective of our study was evaluating the functions of bacterial and protozoan lipoxygenases by evolutionary and taxonomic analysis using bioinformatics tools. Lipoxygenase sequences were identified and examined using BLAST, followed by analysis of constructed phylogenetic trees and networks. Our results support the theory on the involvement of lipoxygenases in the formation of multicellular structures by microorganisms and their possible evolutionary significance in the emergence of multicellularity. Furthermore, we observed association of lipoxygenases with the suppression of host immune response by parasitic and symbiotic bacteria including dangerous oppor- tunistic pathogens. DOI: 10.1134/S0006297920090059 Keywords: lipoxygenases, bacteria, protozoa, bioinformatics, phylogenetics, signaling, multicellularity, opportunistic pathogens INTRODUCTION The products of lipoxygenase reaction in plants are involved in the organism response to damage and attack Lipoxygenases catalyze oxidation of polyunsaturated by pathogenic microorganisms [9-11]. The most known fatty acids (PUFAs) with the formation of hydroperoxides among them are jasmonates (cyclic oxylipins structurally [1]. Eukaryotic lipoxygenases form a family of proteins similar to animal prostaglandins) that exhibit pronounced with a conserved amino acid sequence. The active site of hormonal activity [10]. these enzymes contains non-heme iron or, rarely, man- In addition to higher plants, lipoxygenases are also ganese [2]. Lipoxygenases are abundant in animals, present in algae and mosses. It has been suggested that plants, and fungi [3, 4], where they perform the same pheromones mediating chemoattraction between male function – synthesis of biologically active compounds and female gametes in brown algae are synthesized via the oxylipins (oxidized PUFAs). lipoxygenase pathway [12]. In mosses, the lipoxygenase Arachidonic acid is the main substrate of vertebrate pathway is likely required for normal development [13]. lipoxygenases. The resulting products – leukotrienes, The most interesting feature of the lipoxygenase hydroxy- and oxo-eicosatetraenoic acids, and lipoxins – pathway in fungi is the presence of manganese lipoxyge- control the inflammatory response, as well as apoptosis, nases (MnLOXs) that contain manganese ion in the thrombocyte function, and tumor development [4-8]. active site instead of iron ion. It is believed that these enzymes function as invasive factors and participate in quorum sensing and morphology switch in dimorphic * To whom correspondence should be addressed. fungi [12]. 1048 FUNCTIONS OF BACTERIAL AND PROTOZOAN LIPOXYGENASES 1049 Hence, lipoxygenases in multicellular organisms are b) invasive growth and disruption of cell membranes by predominately involved in cell-to-cell communication, as the pathogen – this mechanism was suggested for P. well as the processes of antimicrobial defense and micro- aeruginosa; bial aggression. c) evasion of immune response – this strategy was dis- In view of this fact, the presence of lipoxygenases in cussed above for P. aeruginosa; some bacteria and protozoa seems important. Using d) lipoxygenases as oxygen sensors – this function is sug- molecular genetics and bioinformatics approaches, gested for P. aeruginosa lipoxygenase based on its low lipoxygenase genes have been identified in 0.5% of oxygen affinity; sequenced bacterial genomes (as of 2015) [14]. Only few e) detoxification of PUFAs, which are detrimental for of these enzymes have been investigated in vitro, includ- many bacteria. ing lipoxygenases from two cyanobacteria of the Nostoc However, no experimental data have been provided genus [15, 16], cyanobacterium of the Anabaena genus in this work to support one hypothesis or another. [17], Myxococcus xanthus of myxobacteria [18], and Considering an insufficient amount of available Pseudomonas aeruginosa of the pseudomonad group [19, experimental data, it seemed reasonable to conduct phy- 20]. In Protozoa, the lipoxygenase sequence was identi- logenetic and taxonomic profiling of bacterial and proto- fied only in the slime mold Dictyostelium discoideum [3]. zoan lipoxygenases and compare obtained results with the At present, the functions of bacterial and protozoan literature data on the ecophysiology of respective organ- lipoxygenases remain poorly understood [2, 14, 21]. isms. However, only few of such studies have been report- Most of the data available on the lipoxygenase preva- ed so far. lence in bacteria are presented in the review by Horn et al. The review by Horn et al. [14] only presents the tax- [14]; however, no association of their presence with the onomic profile at the phylum level, which does not allow ecophysiology of respective organisms has been exam- elucidating associations with the ecophysiology. Hansen ined. A high prevalence of lipoxygenases in nitrifying bac- et al. [25] conducted phylogenetic profiling of bacterial teria was noted in this review and their association with lipoxygenases, but compared the results with biochemical nitrogen metabolism was suggested [14, 22]. A high rather than ecophysiological data. prevalence of lipoxygenases in cyanobacteria was also The objective of our study was to establish an associ- mentioned, and an attempt was made to relate this fact to ation between the phylogenetic and taxonomic distribu- the Great Oxidation Event caused by their activity [14]. tion of bacterial and protozoan lipoxygenases and eco- However, the biochemical mechanisms behind such asso- physiological features of the organisms. ciation remain obscure. The majority of data on the lipoxygenase functions have been accumulated for the enzyme from the rod- MATERIALS AND METHODS shaped pathogenic bacterium P. aeruginosa. This lipoxy- genase is likely one of the bacterial pathogenic factors. It We searched for potential lipoxygenase sequences was found that it converts host fatty acids into lipoxins with BLAST [26] using UniProt (https://www.uniprot. that exhibit the anti-inflammatory and local immunosup- org/blast/) [27] and NCBI (https://blast.ncbi.nlm. pressive activity. It was assumed based on this fact that P. nih.gov/Blast.cgi) databases. The two databases were aeruginosa uses lipoxygenase to suppress host immunity used to reduce the probability of false negative results. [19, 20]. The data became available recently that another The main search among bacteria was carried out using lipoxygenase isozyme initiates ferroptosis of the bronchial the UniProt database, and the control search was done epithelium by cleaving host cell phospholipids [23]. using the NCBI database. The main search among Horn et al. emphasized in their review that no eukaryotes was performed using the NCBI database, and lipoxygenases have been found in the majority of bacteri- the control one – the UniProt database. The use of dif- al pathogens of humans. In particular, these enzymes are ferent databases for bacteria and protozoa was due to the absent in staphylococci, streptococci, Mycobacterium fact that BLAST UniProt is optimized for visual control tuberculosis and Mycobacterium leprae, Vibrio cholerae, of a large number of alignments (more than 500 for bac- Legionella pneumophila, Helicobacter pylori, and teria), while NCBI is optimal for a targeted search Klebsiella pneumoniae [14]. The authors concluded that among a relatively low number of sequences (which is the the pathogenicity of these bacteria does not require the case for protozoa). presence of lipoxygenase [14]. Lipoxygenase sequences from phylogenetically dis- The existing hypotheses on the functions of bacterial tant organisms in the Swiss-Prot database were used as lipoxygenases were comprehensively summarized by queries: human arachidonate 12-lipoxygenase (UniProt Goloshchapova et al. [24]: ID: P18054) [28], manganese lipoxygenase from the fun- a) cell-cell signaling – this function is postulated for P. gus Gaeumannomyces graminis (UniProt ID: Q8X151) aeruginosa and suggested for myxobacteria demonstrating [29], and
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