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Janthinobacterium Tructae Sp. Nov., Isolated from Kidney of Rainbow Trout (Oncorhynchus Mykiss)

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Janthinobacterium Tructae Sp. Nov., Isolated from Kidney of Rainbow Trout (Oncorhynchus Mykiss) pathogens Article Janthinobacterium tructae sp. nov., Isolated from Kidney of Rainbow Trout (Oncorhynchus mykiss) Won Joon Jung 1,†, Sang Wha Kim 1,†, Sib Sankar Giri 1 , Hyoun Joong Kim 1, Sang Guen Kim 1, Jeong Woo Kang 1, Jun Kwon 1, Sung Bin Lee 1, Woo Taek Oh 1, Jin Woo Jun 2,* and Se Chang Park 1,* 1 Laboratory of Aquatic Biomedicine, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 08826, Korea; [email protected] (W.J.J.); [email protected] (S.W.K.); [email protected] (S.S.G.); [email protected] (H.J.K.); [email protected] (S.G.K.); [email protected] (J.W.K.); [email protected] (J.K.); [email protected] (S.B.L.); [email protected] (W.T.O.) 2 Department of Aquaculture, Korea National College of Agriculture and Fisheries, Jeonju 54874, Korea * Correspondence: [email protected] (J.W.J.); [email protected] (S.C.P.) † Both authors contributed equally. Abstract: This study presents a novel Janthinobacterium strain, SNU WT3, isolated from the kidney of rainbow trout. A phylogenetic study using 16S rRNA sequences indicated that the strain is closely related to Janthinobacterium svalbardensis JA-1T. However, biochemical analysis found differences in D-xylose adonitol, N-acetylglucosamine, arbutin, and cellobiose. As for genome-to-genome distance and average nucleotide identity values calculated between strain SNU WT3 and other related strains such as J. lividum EIF1, J. svalbardensis PAMC 27463, and J. agaricidamnosum BHSEK were all below the cutoff value between species. DNA-DNA hybridization between strain SNU WT3 and other close relatives indicated the results of J. lividum DSM 1522T (47.11%) and J. svalbardensis Citation: Jung, W.J.; Kim, S.W.; JA-1T (38.88%) individually. The major fatty acid compositions of strain SNU WT3 were cylco-C Giri, S.S.; Kim, H.J.; Kim, S.G.; 17:0 Kang, J.W.; Kwon, J.; Lee, S.B.; (41.45%), C16:0 (33.86%) and C12:0 (5.87%). The major polar lipids were phosphatidylethanolamine, Oh, W.T.; Jun, J.W.; et al. phosphatidylcholine, phosphatidylglycerol, and diphosphatidylglycerol. The quinone system was Janthinobacterium tructae sp. nov., composed mainly of ubiquinone Q-8. The genome of strain SNU WT3 consists of 6,314,370 bp with a Isolated from Kidney of Rainbow G + C content of 62.35%. Here, we describe a novel species of the genus Janthinobacterium, and the Trout (Oncorhynchus mykiss). name Janthinobacterium tructae has been proposed with SNU WT3T (=KCTC 72518 = JCM 33613) as Pathogens 2021, 10, 229. https:// the type strain. doi.org/10.3390/pathogens10020229 Keywords: Jantinobacterium; Jantinobacterium tructae; rainbow trout; Oncorhynchus mykiss Academic Editor: Pantelis Katharios Received: 10 November 2020 Accepted: 17 February 2021 1. Introduction Published: 19 February 2021 Members of the genus Janthinobacterium are Gram-negative, rod-shaped, psychrotoler- Publisher’s Note: MDPI stays neutral ant bacteria normally found in environments such as soil, water, and the Arctic glaciers [1,2]. with regard to jurisdictional claims in Janthinobacterium lividum, one of the earliest discovered Janthinobacterium species, was re- published maps and institutional affil- ported in 1978, and the species is found frequently in our nearest environment, including iations. green onions, salad mix, water, and soil [3,4]. Since the discovery of J. lividum, only a few more Janthinobacterium species have been reported. Jantinobacterium agaricidamnosum was isolated in 1999 and is known to cause soft rot disease of the mushroom Agaricus bisoporus [5]. Janthinobacterium svalbardensis was identified in 2013, isolated from ice samples of the island Spitsbergen in the Arctic [6]. Janthinobacterium psychrotolerans S3-2T, isolated from a fresh- Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. water pond near Aarhus, Denmark, was described in 2017 [7]. Three more species were de- This article is an open access article scribed in 2020 from tropical and subtropical rivers of China: Janthinobacterium violaceinigrum T T T distributed under the terms and FT13W , Janthinobacterium aquaticum FT58W , and Janthinobacterium rivuli FT68W [8]. conditions of the Creative Commons Only a few studies have described Janthinobacterium species as a pathogen. The species Attribution (CC BY) license (https:// was considered nonpathogenic to humans until the first report of septicemia in Thailand in creativecommons.org/licenses/by/ 1992 [9]. Some studies also describe Janthinobacterium as a fish pathogen, mostly affecting 4.0/). the rainbow trout (Oncorhynchus mykiss)[10,11]. Pathogens 2021, 10, 229. https://doi.org/10.3390/pathogens10020229 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 229 2 of 13 Pathogens 2021, 10, x FOR PEER REVIEW 2 of 13 Since not many Janthinobacterium species have been identified, only a few studies have been published about them. Despite this, the violacein complex of the Janthinobac- teriumof septicemiathat consists in Thailand of the in genes 1992 [9].vioA Some, vioB studies, vioC also, describevioD, and JanthinobacteriumvioE has been as a thefish focus of considerablepathogen, mostly research affecting [12,13 the]. rainbowJ. lividum troutis (Oncorhynchus well known mykiss for) [10,11]. producing pigment [2,14]. Since not many Janthinobacterium species have been identified, only a few studies As the compound violacein, which induces purple pigmentation, has distinctive antivi- have been published about them. Despite this, the violacein complex of the Janthinobacte- ral, antibacterial,rium that consists and of the antifungal genes vioA properties,, vioB, vioC, vioDJ. lividum, and vioEhas has been been usedthe focus for of the con- treatment of Batrachochytriumsiderable research dendrobatidis[12,13]. J. lividuminfection is well known in amphibians for producing [15 ].pigment Among [2,14]. the As strains the which werecompound described violacein, in 2020, whichJanthinobacterium induces purple pigmentation, violaceinigrum hasFT13W distinctiveT and antiviral,Janthinobacterium anti- rivulibacterial,FT68W andT produce antifungal violacein properties, [ 8J.]. lividum However, has been not used all for Janthinobacteria the treatment of Batracho- produce viola- cein.chytriumJ. agaricidamnosum dendrobatidis infectionis a non-pigmented in amphibians soft [15]. rot Among pathogen the strains [5]. J. which svalbardensis were de-produces scribed in 2020, Janthinobacterium violaceinigrum FT13WT and Janthinobacterium rivuli dark red-brownT to black pigmentation, which was designated as a violacein-like pigment, FT68W produce violacein [8]. However, not all Janthinobacteria produce violacein.T J. differentagaricidamnosum from the purpleis a non-pigmented pigmentof softJ. rot lividum pathogen[6]. [5].J. psychrotolerans J. svalbardensis producesS3-2 lacks dark the abil- ity tored-brown produce to violacein black pigmentation, but shows which antibiotic was designated resistance, as a violac incompleteein-like pigment, denitrification, dif- and fermentationferent from [ 7the]. purple pigment of J. lividum [6]. J. psychrotolerans S3-2T lacks the ability to produceIn this violacein study, we but isolated shows antibiotic a novel resistance, pathogen, incomplete SNU WT3, denitrification, from the and swollen fermen- kidney of diseasedtation rainbow [7]. trout (Oncorhynchus mykiss) that exhibited abnormal swimming behavior from a farmIn this in study, the Republic we isolated of a Korea. novel pathog The identificationen, SNU WT3, offrom the the bacterium swollen kidney was performedof diseased rainbow trout (Oncorhynchus mykiss) that exhibited abnormal swimming behav- using 16S rRNA gene-based phylogenetic analysis, biochemical analysis, chemotaxonomic ior from a farm in the Republic of Korea. The identification of the bacterium was per- characteristics,formed using and 16S completerRNA gene-based genome phylogenet analysis.icWe analysis, present biochemical the genome analysis, of strain chemo- SNU WT3 as welltaxonomic as its phenotypic characteristics, features and complete and classification. genome analysis. We present the genome of strain SNU WT3 as well as its phenotypic features and classification. 2. Results 2.1. Bacterial2. Results Characteristics 2.1.1.2.1. Histopathology Bacterial Characteristics 2.1.1.Intensive Histopathology necrotic changes in hematopoietic tissues of the kidney and spleen were observed.Intensive Karyolysis, necrotic pyknosis, changes in karyorrhexis, hematopoietic tissues and hydropic of the kidney and and vacuolar spleen degenerationwere occurredobserved. to interstitialKaryolysis, pyknosis, hematopoietic karyorrhexis cells, ofand the hydropic kidney and (Figure vacuolar1A). degeneration In renal tubules, occurred to interstitial hematopoietic cells of the kidney (Figure 1A). In renal tubules, ep- epithelialithelial cellcell pyknosis and and eosinophilic eosinophilic droplet droplet accumulation accumulation existed. Hyperemia existed. and Hyperemia mel- and melanomacrophageanomacrophage accumulation accumulation in the in interstiti the interstitiumum could also could be observed. also be observed.Hematopoietic Hematopoi- etic tissue of of the the spleen spleen showed showed eosinophilic eosinophilic staining stainingand the features and the of karyorrhexis, features of kary- karyorrhexis, karyolysis,olysis, and and pyknosis, pyknosis, indicating indicating a wide a range wide of range tissues of are tissues in the process are in theof necrosis process (Fig- of necrosis (Figureure1 1B).B). Figure
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