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Biological Work on Medically Important Nocardia Species

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Biological Work on Medically Important Nocardia Species Actinomycetologica (2007) 21:46–51 Copyright Ó 2007 The Society for Actinomycetes Japan VOL. 21, NO. 1 Award Lecture Biological Work on Medically Important Nocardia Species Yuzuru Mikami Research Center for Pathogenic Fungi and Microbial Toxicoses, Chiba University, 1-8-1, Inohana, Chuo-ku, Chiba 260-8673, Japan (Received May 1, 2007 / Accepted May 1, 2007 / Published Jun. 7, 2007) INTRODUCTION Nocardia is an aerobic Gram-positive, filamentous and partially acid-fast bacterium, which is classified among the Human nocardioses are caused by members of the pathogenic actinomycetes. Among the Nocardia species, Nocardia species. Coupled with the increasing number N. asteroides complex (N. asteroides sensu strict, N. far- of the immunocompromised patients who are treated with cinica and N. nova), N. brasiliensis, N. otitidiscaviarum, steroids or broad-spectrum antibiotics, and of AIDS and N. transvalensis, N. cyriacigeorgica, N. asiatica, and N. organ transplant patients, the incidence of infection is beijingensis cause human infections. Reportedly, infec- increasing1–3). Concomitant with introduction of new ge- tion caused by Nocardia is uncommon, and has been netic technologies for Nocardia classification, reports of considered to be rare8,9). However, coupled with the new species of Nocardia have increased: during 2004 increasing number of the immunocompromised patients 2007, more than 40 species were established4). treated with steroids, AIDS, and organ transplant patients, Our recent phylogenetic studies of these clinical the frequency of cases of nocardiosis is increasing in Nocardia isolates have suggested the presence of many Japan. new species among the isolated strains. Detailed taxonomic Taxonomic studies of these Nocardia clinical isolates studies have identified more than 17 new Nocardia spe- revealed more than 17 new Nocardia species and three cies5). Nocardia species show species-specific drug sus- new species of Gordonia strains. Nocardia is known to ceptibility patterns; consequently, development of simpler have species-specific drug-resistance patterns, and we had and more rapid identification methods is expected because reported various novel resistance mechanisms, including identification is necessary to initiate proper antibiotic glucosylation, phosphorylation, and ribosylation of rifam- therapy. In 2004, whole-genome analysis of N. farcinica picin. This constitutes the first report of ribosylation as an was completed; that information was publicized6). That antibiotic resistance mechanism. genomic information engendered discovery of new sec- During the course of our screening program for new ondary metabolites such as siderophore compounds, which bioactive metabolites including immunosuppressive, anti- have been considered to be related to virulence factors in fungal, and other bioactive compounds, those compounds pathogenic bacteria. were isolated and their structures and biological activities New sources of bioactive materials such as marine were determined. Our studies of biologically active organisms and new microbes from different ecological metabolites using clinical isolates of Nocardia species niches have promoted recent advances in the discovery of revealed more than 20 new bioactive compounds with new drugs. However, such attention has never been paid unique structures and biological activities. to pathogenic microbes such as pathogenic Nocardia.We continue our interest in biologically active compounds from PROPOSAL OF NEW SPECIES pathogenic microorganisms, especially from pathogenic OF NOCARDIA ISOLATED FROM microorganisms because: i) pathogenic microorganisms CLINICAL SAMPLES IN JAPAN should have unique competition mechanisms between path- ogenic microbes and other microbes, plants, and animals; In 2004, we proposed one new species of Nocardia: ii) pathogenic microbes have never been considered to be N. asiatica10). Thereafter, we proposed more than 16 new new sources of biologically active metabolites; and iii) species of Nocardia (Fig. 1): N. anaemiae, N. aobensis, pathogenic microbes should be biologically more active N. araoensis, N. arthritidis, N. concave, N. exalbida, N. and have different metabolic pathways than those of non- higoensis, N. inohanensis, N. niigatensis, N. pneumoniae, pathogenic microbes. Furthermore, 60–100 strains of N. shimofusensis, N. sienata, N. testacea, N. thailandica, pathogenic Nocardia have been referred to our research N. vermuculata, and N. yamanashiensis11–14). Recently, center every year for identification from clinical laborato- we also proposed one new species of Nocardia: N. ries in Japan, and the numbers of the maintained cultures terpenica5). In addition to a new species of Nocardia, are increasing7). These facts have stimulated our screening we also proposed three new species of Gordonia which studies of secondary active metabolites from these patho- were isolated from Japanese patients: G. araii, G. effuse genic Nocardia8). and G. otitidis15,16). 46 ACTINOMYCETOLOGICA VOL. 21, NO. 1 R. opacus DSM43205 N. globerula DSM46019 N. corynebacterioides DSM20151 N. asiatica IFM0245 N. pneumoniae IFM0784 62 N. beijingensis AS4.1521 97 75 N. araoensis IFM0575 68 N. arthritidis IFM10035 N. puris DSM44599 N. shimofusensis IFM10311 94 N. higoensis IFM10084 N. farcinica ATCC3318 N. transvalensis DSM43405 100 N. asteroides ATCC19247 N. brasiliensis DSM43758 N. tenerifensis taxon: 228006 N. takedaensis MS1-3 N. abcessus JCM6043 N. cyriacigeorgica DSM43758 N. pigrifrangens 7031 N. flavorosea 100 JCM3342 58 N. carnea DSM43397 N. sienata IFM10088 T 100 N. testacea IFM0937T N. brevicatena DSM43024 100 N. paucivorans DSM44386 N. neocaledoniensis SBHR OA6 N. caishijiensis F829 N. novocastrensa N1251 100 N.thailandica IFM10145T N. pseudobrasiliensis DSM44290 T N. crassostreae JCM10500 N. seriolae JCM336 N. niigatensis IFM0330 N. inohanensis IFM0092 99 N. yamanashiensis IFM0265 N. uniformis DSM43136 T 60 N. otitidiscaviarum NCTC1934 T N. nova JCM6044 100 N. pseudosporangifera JCM3288 N. vermiculata IFM0391T 60 N. vaccinii DSM43285 58 N. africana DSM44491 N. cerradoensis Y9 100 63 N. veterana DSM44445 95 N. kruczakiae MB2876 N. vinacea MK703-102F1 67 N. pseudovaccinii DSM43406 68 N. anaemiae IFM0323 T (AB162801) N. xishanensis AS4.1860 N. alba YIM30243 77 N. devorans N1086 93 N. ignorata DSM44496 N. salmonicida 100 JCM4826 93 N. fluminea DSM44489 N. cummidelens DSM4490 100 N. soli DSM44488 0.01 Fig. 1. Newly proposed Nocardia species by our research laboratory. NOVEL ANTIBIOTIC RESISTANCE MECHANISMS Rifampicin is a valuable chemotherapeutic agent that is used to combat infections such as tuberculosis, staph- ylococcal infections, and some infections caused by Gram-negative organisms17,18). After the introduction of rifampicin to clinical practice in 1972, resistant strains came to be identified19). Classically, microbes resist the action of antibiotics by target-site alteration. This was 20) true in rifampicin in M. tuberculosis . Another way in Fig. 2. Inactivation of rifampicin by glucosylation, phosphory- which bacteria might respond to antibiotic challenge occurs lation or ribosylation in pathogenic actinomycetes. by inactivation of the drug21). We had reported three new inactivation mechanisms: decomposition, glucosylation, and phosphorylation (Fig. 2) in pathogenic actinomy- M. avium, and M. parafortuitum. The DNA from M. cetes22–24). In addition, ribosylation has been identified for smegmatis DSM 43756 responsible for this phenotype some fast-growing Mycobacterium species: M. smegmatis, was cloned and characterized. Biochemical studies showed 47 ACTINOMYCETOLOGICA VOL. 21, NO. 1 Fig. 3. ADP ribosylation of a new inactivation mechanism of rifampicin by Mycobacterium smegmatis. that the gene encoded a mono-ADP-ribosyltransferase; siliensis strains and that other Nocardia strains are it was therefore designated as adr for ADP-ribosylation useful sources for the screening of bioactive compounds. of rifampicin (Fig. 3)25). The enzyme consists of 143 N. brasiliensis IFM 0089 produced new cytotoxic anti- amino acids and has a molecular weight of 15.9 kDa. biotics named brasiliquinones A, B and C29). Brasiliqui- In vitro experiments revealed that NAD is the preferred nones are unique benz[a]anthraquinone antibiotics with an cofactor for inactivation. During our characterization of ethyl group at the C-3 position29). Three new compounds, IN53, a class-1 plasmid-located and composite transposon- nocarasins A, B and C, were isolated from N. brasiliensis located integron of Escherichia coli which carries an IFM 067730). Nocaracins are new benzenoid metabolites unusual array of gene cassettes, this bacterium was found with a geranyl side chain. Nocaracins showed inhibitory to have a gene that is responsible for rifampicin inacti- activity against some Gram-positive bacteria, especially vation19). acid-fast bacteria such as N. asteroides and Mycobacterium smegmatis30). BIOACTIVE SECONDARY METABOLITES Brasilinolides are new 32-membered macrolides with a FROM PATHOGENIC NOCARDIA tetrahydropyrane ring and a 2-deoxypyranose moiety from the broth of N. brasiliensis IFM 040631). Brasilinolides Our continuing studies of bioactive metabolites from exhibit potent immunosuppressive activity in mouse pathogenic Nocardia have revealed new bioactive metab- mixed-lymphocyte assay and antifungal activity against olites from Nocardia clinical isolates; we found that most Aspergillus niger (Fig. 4)31). A novel tricyclic metabolite N. brasiliensis strains produce antibacterial compounds with potent immunosuppressive
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