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Arthrobacter Flavus Sp. Nov., a Psychrophilic Bacterium Isolated from a Pond in Mcmurdo Dry Valley, Antarctica

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Arthrobacter Flavus Sp. Nov., a Psychrophilic Bacterium Isolated from a Pond in Mcmurdo Dry Valley, Antarctica International Journal of Systematic and Evolutionary Microbiology (2000), 50, 1553–1561 Printed in Great Britain Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica G. S. N. Reddy,1 R. K. Aggarwal,1 G. I. Matsumoto2 and S. Shivaji1 Author for correspondence: S. Shivaji. Tel: j91 40 7172241. Fax: j91 40 7171195. e-mail: shivas!ccmb.ap.nic.in 1 Centre for Cellular and CMS 19YT, a psychrophilic bacterium, was isolated from a cyanobacterial mat Molecular Biology, Uppal sample from a pond in Antarctica and was characterized taxonomically. The Road, Hyderabad 500 007, India bacterium was aerobic, Gram-positive, non-spore-forming, non-motile, exhibited a rod–coccus growth cycle and produced a yellow pigment that was 2 Department of Environmental Information insoluble in water but soluble in methanol. No growth factors were required Science, Otsuma Women’s and it was able to grow between 5 and 30 SC, between pH 6 and pH 9 and University, Tamashi, Tokyo tolerated up to 115% NaCl. The cell wall peptidoglycan was Lys-Thr-Ala3 (the 206, Japan A3α variant) and the major menaquinone was MK-9(H2). The GMC content of the DNA was 64O2 mol%. The 16S rDNA analysis indicated that CMS 19YT is closely related to group I Arthrobacter species and showed highest sequence similarity (9791%) with Arthrobacter agilis. Furthermore, DNA–DNA hybridization studies also indicated 77% homology between CMS 19YT and A. agilis. It differed from A. agilis, however, in that it was psychrophilic, non- motile, yellow in colour, exhibited a rod–coccus growth cycle, had a higher degree of tolerance to NaCl and was oxidase- and urease-negative and lipase- positive. In addition, it had a distinct fatty acid composition compared to that of A. agilis: the predominant fatty acids were C15:0, anteiso-C15:0,C16:0, iso-C16:0, T C17:0, anteiso-C17:0 and C18:0. It is proposed, therefore, that CMS 19Y should be placed in the genus Arthrobacter as a new species, i.e. Arthrobacter flavus sp. nov. The type strain of A. flavus is CMS 19YT(l MTCC 3476T). Keywords: Arthrobacter, psychrophile, Antarctica, halotolerant, yellow pigment INTRODUCTION teristics (Keddie et al., 1986) such as morphology, physiological properties, cell wall composition, GjC Members of the genus Arthrobacter constitute a content of the DNA (mol%), menaquinone type, predominant group of micro-organisms in soils from nutritional requirements, antibiotic sensitivity and various parts of the world. In addition to mesophilic biochemical test results (Johnson et al., 1981; Johnson arthrobacters (Schleifer & Kandler, 1972; Keddie & Bellinoff, 1981; Shivaji et al., 1989a). Despite these & Jones, 1981; Keddie et al., 1986), psychrophilic similarities, the above Antarctic strains differed from arthrobacters have been reported from samples of the mesophilic species of Arthrobacter in that they subterranean cave silts (Gounot, 1967), glacier silts were all psychrophilic, contained glucose as the cell (Moiroud & Gounot, 1969) and the soils of Antarctica wall sugar and did not hydrolyse starch. Pigmented (Johnson et al., 1981; Johnson & Bellinoff, 1981; Arthrobacter strains containing -diaminopimelic Madden et al., 1979; Siebert & Hirsch, 1988; acid (-DAP) in the cell wall have also been reported Shivaji et al., 1989a). The psychrophilic isolates of from Antarctic soils (Siebert & Hirsch, 1988). Many of Arthrobacter from Antarctica were identified on the these Arthrobacter strains from Antarctica are unique basis of numerous phenotypic genus-specific charac- in that they are psychrophilic and possess phenotypic ................................................................................................................................................. traits by which they differ from the mesophilic Arthro- Abbreviations: DAP, diaminopimelic acid; NJ, neighbour- bacter strains; thus they cannot be affiliated to any of joining; UPGMA, unweighted pair group method with averages. the known species. These isolates were tentatively The EMBL accession number for the 16S rDNA sequence of CMS 19YT is assigned to a group in the genus Arthrobacter known AJ242532. as the Arthrobacter simplex\tumescens group (Keddie 01262 # 2000 IUMS 1553 G. S. N. Reddy and others & Jones, 1981; Johnson et al., 1981; Johnson & peptidoglycan. It differed, however, from all of the Bellinoff, 1981; Siebert & Hirsch, 1988). Arthrobacter reported mesophilic and psychrophilic species with simplex and Arthrobacter tumescens have now been respect to many characteristics and was therefore reclassified as Pimelobacter simplex and Pimelobacter designated as a new species, for which we propose the tumescens (Suzuki & Komagata, 1983a, b). name Arthrobacter flavus sp. nov. All of the species of the genus Arthrobacter are Gram- positive, catalase-positive, aerobic and asporogenous METHODS bacilli with a coryneform morphology (Schleifer & Source of the organism, media and growth conditions. Kandler, 1972) and have been separated into two Cyanobacterial mat samples were collected during the groups on the basis of their peptidoglycan, which austral summer from the shores of an unnamed pond, contains lysine as the diamino acid. Group I species of designated E4 (77m 31h 7d S, 160m 45h 4d E), from the labyrinth Arthrobacter contain the A3α peptidoglycan variant in of the Wright Valley, a constituent valley of McMurdo Dry which cross-linkage of murein is brought about by Valley, Antarctica (Matsumoto, 1993; Matsumoto et al., interpeptide bridges involving monocarboxylic - 1993). The sample was initially analysed microscopically amino acids or glycine or both, as observed in most (i1000) and found to contain Phormidium laminosum as the species of Arthrobacter including Arthrobacter globi- most abundant cyanobacterium and also contained some formis, the type strain of the genus (Stackebrandt et al., green algae (Matsumoto et al., 1993). 1983). The group II species of Arthrobacter possess the For the detection of bacteria, a piece of the above cyano- A4α peptidoglycan variant in which the peptidoglycan bacterial mat sample (approx. 200 mg) was suspended in type is -Lys-Ala-Glu, as in Arthrobacter nicotianae, a tube containing 1 ml sterile saline (150 mM NaCl), Arthrobacter uratoxydans, Arthrobacter protophormiae teased with a glass rod and vortexed for approximately et al 2–5 min to obtain a suspension. An aliquot of the suspension (Schleifer & Kandler, 1972; Stackebrandt ., 1983), (100 µl) was plated on Antarctic Bacterial Medium (ABM) Arthrobacter sulfureus or -Lys--Glu, as in plates containing 0n5% (w\v) peptone, 0n1% (w\v) yeast (Stackebrandt et al., 1995; Funke et al., 1996). Re- extract and 1n5%(w\v) agar (pH 6n9) and incubated at 10 mC cently, Arthrobacter rhombi, a new species (isolated (Shivaji et al., 1988, 1989a, b, 1991, 1992). The appearance of from Greenland halibut) with A4α peptidoglycan, was colonies was monitored on a regular basis and pure cultures also included in Arthrobacter group II (Osorio et al., of the bacteria were established. One of the pure cultures 1999). Phylogenetic studies indicate that certain Micro- thus established was yellow in colour and was designated CMS 19YT. The optimal temperature, pH and salt con- coccus species such as Micrococcus agilis, Micrococcus T lylae and Micrococcus luteus are intermixed with the centration for the growth of CMS 19Y were determined by species of Arthrobacter (Stackebrandt et al., 1995) and using ABM plates. detailed phylogenetic analysis along with phenotypic Morphology and motility tests. Cultures of CMS 19YT in the similarities have resulted in the reclassification of M. lag-, log- and stationary phases of growth were observed agilis as Arthrobacter agilis (Koch et al., 1995). The under a phase-contrast microscope (1000i) to ascertain genus also includes a number of other species for their shape and motility. Motility was also determined by the which the chemotaxonomic data are lacking, e.g. hanging drop method and staining of the flagellum was done by the method of silver impregnation (Blenden & Goldberg, Arthrobacter mysorens, Arthrobacter picolinophilus, 1965) using Pseudomonas aeruginosa as a positive control. Arthrobacter radiotolerans and Arthrobacter sidero- capsulatus (Keddie et al., 1986). Detailed studies have Biochemical characteristics. All of the tests were performed now reclassified A. picolinophilus as Rhodococcus by growing the culture at 20 mC in the appropriate medium. erythropolis (Koch et al., 1995) and A. radiotolerans as The activities of catalase, oxidase, phosphatase, gelatinase, urease, arginine dihydrolase and β-galactosidase were de- Rubrobacter radiotolerans (Suzuki et al., 1989). It has termined according to standard methods (Holding & Collee, also been shown that A. mysorens is distinct from 1971). The production of indole, the utilization of citrate, the the Arthrobacter species recognized up to 1983 reduction of nitrate to nitrite and the hydrolysis of starch, (Stackebrandt et al., 1983). Furthermore, many other aesculin and Tween 80 were measured according to the species that were included in the genus Arthrobacter procedures described elsewhere (Stanier et al., 1966; Holding (e.g. Arthrobacter duodecadis, Arthrobacter viscosus, & Collee, 1971; Stolp & Gadkari, 1981). The utilization of Arthrobacter variabilis, A. simplex and A. tumescens) six different sugars, leading to the formation of acid with or have now been excluded since they contain meso-DAP without gas production, was monitored according to Hugh or -DAP in the
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