The Korean Journal of Microbiology, Vol. 43, No. 3, September 2007, p. 193-200 Copyright 2007, The Microbiological Society of Korea w üy œ» ³ ³ p ½ù 1 Á½ 1 Á½ ³ 2 Á 2 Á½ 1,2 * w w w w w w w 3œ, ƒ w œ» ³ ³ wš, w z w. ³ ³ s œ»» w, ³ ³ d ƒƒ plate count agar dichloran rose bengal chloramphenicol agar w. w» ³ 168~3,887 MPN/m 3, 168~6,339 MPN/m 3, ³ 34~389 MPN/m 3, 91~507 MPN/m 3, y w d r ³ ³ j ùkû. w ³ 84%, xw ³ 61% Micrococcus, 75% M. luteus y, Staphylococcus 10%. Micrococcus ƒ, w w ù s w p ³ œ» d. s w l 15 ³ y w, Cladosporium, Aspergillus, Penicillium w ³ 69% w. 1 w Stachybotrys, S. chartarum ³ w. ¾ Aspergillus, Penicillium, Stachybotrys w, w ³, œ» ³ ³ w ƒ v w š q. Key words ý airborne bacteria, airborne fungi, elementary school, indoor air ³ ³ ü, l x, ù wœ k, w, y œ» ³ ³ s w ƒwš (1, 4, 7, 12, 13). y,» ww xk bioaerosol x w œ». œ»,,, mw ù w, ü y œ» w œ» y w š w w» ƒ w (19). p ü œ» ³ ³ y» y, ³ ü (endotoxin) rp e, ³ w y (23). ü y œ» e w w sƒ, ³(mold) w š (8, 11, 12, 14, 16, 22, 26). w sƒ» w ³ x» wš k, w ³» w ww (14, 22, 26), ³ (mycotoxin) sƒ w œ» ³ w w š (6, 11). w ü œ» w w *To whom correspondence should be addressed. Tel: 82-52-259-2387, Fax: 82-52-259-1694 E-mail: jkim@ulsan.ac.kr z w e (9, 11). w w y ü œ» y w e w, w y œ» y» y w šwš (9, 14, 17, 18, 22, 25). w y ³, y», k ƒ, w w yw œ» w y ü œ» w sƒƒ v w. w ü y œ» e w w sƒ w m y œ» w w ƒ w. w e œ» s, Áš w y œ» s w ww tw (1, 4), w ü œ» ƒ w ³ ³ wš, w ³ ³ w p š w. œ» ³ ³ s 2005 11 12 Ÿ 3 w (BG-E, SH-E, SJ-E) œ» s w, 1 w (BG-E) w (2006 1 ) 193
194 Na Yeong Kim et al. Kor. J. Microbiol œ» s w. w» s ( 10:00~11:40), ( 11:40~ z 12:30), š z( z 3:30~4:30) w 3z ww. œ w gj p» y» mw y» w, BG-E t» ƒ wš. 2w s w, w BG-E 19 š, SH-E SJ-E ƒ 30 35. œ» œ»»(air-ideal, bio-merieux, France) w, l 1.5 m 30 L 300 L œ» g s w. ü d w» w, 10 µm w (PM 10 ) (total particles) s { d»(dustmate, Turnkey Instrument, UK) w 10 z 4 ¾ 6 w d w. œ» ³ ³ ƒ w œ» ³ ³ d ƒƒ plate count agar (agar, 15.0 g; tryptone, 5.0 g; yeast extract, 2.5 g; glucose, 1.0 g; water, 1 L) dichloran rose bengal chloramphenicol(drbc) agar(agar, 15.0 g; glucose, 10.0 g; peptone, 5.0 g; KH 2 PO 4, 1.0 g; MgSO 4 7H 2 O, 0.5 g; rose bengal, 0.025 g; dichloran, 0.002 g; chloramphenicol, 0.1 g; water, 1 L) w ww (5). z, plate count agar 35 C o 48 z ù w š, DRBC agar 25 o C 120 z ùkù w. œ» ³, w» 30 L, w 300 L œ» w s w œ»» œ» 3 1m w y e(most probable number, MPN) y w w š, œ» ³ 300 L œ» s w» w y w.» MPN m v w ùkü. w œ» y ( ü ) y q w» w Windows SPSS v.10.0 w Spearman (r s ) w. œ» ³ ³ ³ ³ 1 w (BG-E) s w w. plate count agar ù w w z, x mw ³ xk p w (20). ³ Staphylococcus, Micrococcus ƒ w API Staph kit, ³ API 20NE kit API 20E kit (biomerieux, France) w w, y (% id) 90% ³ kw w. API kit y 90% ƒ 16S rrna r w. w, nested PCR mw 16S rrna V3 sw, 1 PCR 27f (5'-AGA GTT TGA TCC TGG CTC AG-3') 1492r (5'-GGT TAC CTT GTT ACGA CTT-3') primer w š, 2 s 341f (5'-CCT ACG GGA GGC AGC AG-3') 518r (5'-ATT ACC GCG GCT GCT GG-3') primer w. sw 16S rrna r y DNA»(Applied Biosystems 3100) w ww.» BLAST» w query ƒ similarity 3-4 w z w w ³ y w,» w API kit w, yw x ww. ³, ƒ w w z, xk p lactophenicol cotton blue z x w s û xk p» w ¾ w (21, 27). œ» ³ w» d w, BG-E 25~27 o C, SH-E 14~15 o C, SJ-E 16~20 o C, BG-E 12 ~13 o C, SH-E 11~14 o C, SJ-E 10~11 C o. BG-E 39~41%, SH-E 62%, SJ-E 45~56% d š, BG-E 40~41%, SH-E 62~69%, SJ-E 46~48%, j. w BG-E d w ƒƒ 25 C o 10 C o, ƒƒ 50% 73%. Plate count agar ³» w w w œ» ³ Fig. 1 ùkü. w d y w, 1,392~2,329 MPN/m (s³ 3 1,959 MPN/m 3 ), 428~3,887 MPN/m (s³ 3 1,675 MPN/m 3 ), z 168~288 MPN/m (s³ 3 214 MPN/m ) 3, w z, 219~1,547 MPN/m (s³ 3 808 MPN/m 3 ), 590~6,339 MPN/m (s³ 3 3,721 MPN/m 3 ), 449 MPN/m ) 3, z 168~855 MPN/m (s³ 3 ƒ (Fig. 1). ³ w, w s³» 2.4 ù ƒ 2.2 (Fig. 1). w w w BG-E d w œ» ³, ƒƒ 3 108 MPN/m 71 MPN/ m 3, w» 8%( ) 5%( ) û (Fig. 1). wr ³ ü Spearman (r s ) 0.78(P<0.05) š, 0.64(P<0.01). œ» ³ DRBC agar ³» w w
Vol. 43, No. 3 w œ» ³ ³ 195 Fig 1. Concentration of airborne bacteria at classrooms (A) and corridors (B) of three elementary schools with different situations. Fig. 2. Concentration of airborne fungi at classrooms (A) and corridors (B) of three elementary schools with different situations. œ» ³, 75~216 MPN/m 3 (s³ 161 MPN/m 3 ), 79~389 MPN/m (s³ 3 203 MPN/ m 3 ), z 34~139 MPN/m (s³ 3 84 MPN/m ) 3, w z ƒ û, 110~507 MPN/m (s³ 3 304 MPN/m 3 ), 79~425 MPN/ m (s³ 3 291 MPN/m 3 ), z 91~185 MPN/m (s³ 3 147 MPN/m ) 3 (Fig. 2). ³ y ³ ƒ d, 1.4~2.6, 1.0~2.6, z 1.2~2.7 (Fig. 2). w w w BG-E œ» ³ 24 MPN/m 3, ƒ 3 56 MPN/m d, 2.4 (Fig. 2). wr w ü œ» ³ ü (r s =0.44, P<0.05) š, œ» ³ ³ (r s ) 0.57 (P<0.01) ùkü. œ» w» 6 w w (PM 10 ) BG-E 166 µg/m 3, SH-E 79 µg/m 3, š SJ-E 213 µg/m 3, BG-E 301 µg/m 3, SH-E 152 µg/ m 3, š SJ-E 401 µg/m 3, 52~54% w (Fig. 3). w BG-E d w 36 µg/m 3 w» d 22%, 58 µg/m 3 w» d 19%. w ( 10:00~11:40), ( 11:40~ z 12:30), š z( z 3:30~4:30) w d w, 69~582 µg/m 3, 107 ~324 µg/m 3, z 26~33 µg/m 3, 97~185 µg/m 3, 105~366 µg/m 3, z 19~25 µg/m 3, z ƒ û ùkü (Fig. 3). d» d s ú ww w, w. œ» ³ œ w (BG-E, SH-E, SJ-E) w» 30 L œ» ³ s w plate count agar ù 1,326 (BG-E 491, SH-E 610, SJ-E 225 ), plate count agar w 209 (BG-E 70, SH-E 91, SJ-E 48 ). mw xk p y w, ³ 175
196 Na Yeong Kim et al. Kor. J. Microbiol Fig. 3. Average (6 hr) particulate concentration at classrooms and corridors (A), and PM 10 concentration at classrooms (B) and corridors (C) of three elementary schools. 84% w š, 34 16%. w 300 L s w w 35 28 (80%), 7 (20%). ³ s, y y w. w» BG-E œ» ³ l 70, API kit w, yw p 16S rrna gene x ww (Table 1). 70 s w 32, s w 38, 56 (80%), 14 (20%) w. s w œ» ³ l 9, 13 ³ y w, ³ Micrococcus 43 ƒ xw 61% w, w API Staph kit (Micrococcus spp.)¾ y (Table 1). Staphylococcus 10% 7, S. aureus 4, S. hepidermidis, S. hominis, S. sciuriƒ ƒ 1 s š, Kocuria varians/rosea 4. ù 2, w 16S rrna r Arthrobacter spp., Micrococcus spp. 100% similarity ù, API kit w 2 y, w 1 API kit x z qw xw. ³ Pasteurella 4 6% w, P. haemolytica 2, P. aerogenes 1 (Table 1). Sphingomonas Chryseobacterium ƒ 3 4% w š, S. paucimobilis 3, C. indogenes 2, C. meningosepticum 1 s. Brevundimonas vesicularis, Chryseomonas luteola, Stenotrophomonas maltophilia ƒ 1 š, 1 1 x z ³ w y w w (Table 1). ƒ Micrococcus z s w. Micrococcus spp. ³ ¾ y w» w ƒ yw, x ww, w 20 ³ 15 Micrococcus luteus, 4 M. roseus, š 1 M. agilis y. œ» ³ w» ³ d w DRBC agar l w BG-E 78, SH-E 71, SJ-E 65 214 ³. s w 90, s w 124, ³ xk p» w ¾ w (Table 2). 214 l 15 ³ y w, Cladosporium 81 ƒ 38% š, Aspergillus 34 16%, Penicillium 32 15%, 69% w (Table 2). Paecilomyces Ulocladium ƒƒ 6, Acremonium 5, Alternaria Fusarium ƒƒ 4, Mucor Trichoderma ƒƒ 3 y. Aureobasidium, Curvularia, Scopulariopsis, Stachybotrys ƒƒ 2, Botrytis 1. 8 yeast w w š, 9% w w 19 w y w (Table 3). ³ s w, Cladosporium 90 31 (34%), 124 50 (40%) ƒ š, Aspergillus 12 (13%), 22 (18%)., Penicillium 15 (17%), 17 (14%) ƒ (Table 2). Botrytis Stachybotrys
Vol. 43, No. 3 w œ» ³ ³ 197 Table 1. Tentative identification of airborne bacteria (BG-E) Sampling location and situation (# of colonies examined) Gram stain Identification (# of colonies) Classroom (32) Corridor (38) At class (17) Gram + Micrococcus spp. (10) Staphylococcus aureus (3) Staphylococcus epidermidis (1) Unidentified (1) Gram - Pasteurella spp. (1) Sphingomonas paucimobilis (1) At lunchtime (11) Gram + Micrococcus spp. (9) Unidentified (1) Gram - Sphingomonas paucimobilis (1) After class (4) Gram + Kocuria varians/rosea (1) Gram - Brevundimonas vesicularis (1) Pasteurella aerogenes (1) Pasteurella haemolytica (1) At class (17) Gram + Micrococcus spp. (10) Kocuria varians/rosea (2) Staphylococcus aureus (1) Staphylococcus sciuri (1) Gram - Chryseobacterium indologenes (1) Chryseomonas luteola (1) Stenotrophomonas maltophilia (1) At lunchtime (20) Gram + Micrococcus spp. (14) Staphylococcus hominis (1) Gram - Chryseobacterium indologenes (1) Chryseobacterium meningosepticum (1) Pasteurella haemolytica (1) Sphingomonas paucimobilis (1) Unidentified (1) After class (1) Gram + Kocuria varians/rosea (1) y, Aureobasidium. w s w, Cladosporium, Aspergillus, Penicillium, Ulocladium, Fusarium w 1z y, Acremonium Stachybotrys BG-E, Botrytis SJ-E. š w ü œ» ³ 108~2,329 MPN/m 3, 71~6,339 MPN/m 3 š, œ» ³ 24~389 MPN/m 3, 59~507 MPN/m 3 d, ³ ³ w y w ƒ { f. w w e š w œ» ³ d 18~762 MPN/m 3, 30~1,800 MPN/m 3 œ» ³ d 32~391 MPN/m 3, 83~225 MPN/m 3 w» ³ 3.5, ³ 2.5 ù, e ü d w œ» ³ 4,149 MPN/m 3 ³ 1,888 MPN/m 3 w» ³ 1.8, ³ 4.9 û (1, 4). w 2w z 1 ƒ z s ( z 4 ) w k, z w d w œ» ³ d w x û. y, mw w œ» w e, w ³ ³ w ƒ. š w (1),
198 Na Yeong Kim et al. Kor. J. Microbiol Table 2. Tentative identification of airborne fungi (BG-E, SH-E and SJ-E) Sampling location and situation (# of colonies examined) Identification (# of colonies) At class (38) Cladosporium spp. (11) Curvularia spp. (1) Aspergillus spp. (9) Fusarium spp. (1) Penicillium spp. (6) Trichoderma spp.(1) Acremonium spp.(2) Ulocladium spp. (1) Mucor spp. (2) Unidentified (4) At lunchtime (29) Cladosporium spp. (9) Scopulariopsis spp. (1) Classroom (90) Penicillium spp. (5) Stachybotrys spp. (1) Aspergillus spp. (2) Trichoderma spp. (1) Paecilomyces spp. (2) yeast (3) Alternaria spp. (1) Unidentified (3) Fusarium spp. (1) After class (23) Cladosporium spp. (11) Botrytis spp. (1) Penicillium spp. (4) Stachybotrys spp. (1) Acremonium spp. (1) yeast (1) Aspergillus spp. (1) Unidentified (3) At class (41) Cladosporium spp. (22) Acremonium spp.(1) Aspergillus spp. (4) Alternaria spp. (1) Penicillium spp. (4) Paecilomyces spp. (1) Aureobasidium spp. (2) Trichoderma spp. (1) Ulocladium spp. (2) Unidentified (3) At lunchtime (44) Cladosporium spp. (12) Curvularia spp. (1) Aspergillus spp. (10) Mucor spp. (1) Corridor (124) Penicillium spp. (8) Paecilomyces spp. (1) Alternaria spp. (2) yeast (3) Ulocladium spp. (2) Unidentified (3) Acremonium spp. (1) After class (39) Cladosporium spp. (16) Scopulariopsis spp. (1) Aspergillus spp. (8) Ulocladium spp. (1) Penicillium spp. (5) yeast (1) Fusarium spp. (2) Unidentified (3) Paecillomyces spp. (2) üy œ» w» 8 y 24 s³ ù y z w w» w, w y d v w š q. wr, w ww œ» ³ w d 7~19,500 CFU/m w 3 (9, 22), ü w ³ w 128~971 CFU/m 3 w (2, 3). ³, 96 d w s³ 500 CFU/ m 3, 4,500 CFU/m 3 š, Connecticut 2 w d w ³ s 2,000~50,000 spore/m 3 (9, 22). 1,717 ww ³ (median) ü 82 CFU/m 3, 540 CFU/m 3 (24). x ü ü œ» ³ w üœ»»,», 800 CFU/m 3 w, œ» ³ w w. w œ» ³ 84%, 16% š, Micrococcus ƒ x ww 61% w
Vol. 43, No. 3 w œ» ³ ³ 199, Micrococcus 75% M. luteus, 20% M. roseus y. š w ³ œ» ³ 62~91%, 60% Micrococcus (1). e Micrococcus œ» ³ 37% ƒ sw (4). Micrococcus z, v š w (15), ü œ» Micrococcus š w. 2 w ww, ³ yk ƒ, œ» ³ w wš (14). w Micrococcus p œ» w w, M. luteus, M. roseus ³ ù y ƒ w w ƒ j s w ü ƒ w w. y œ» Micrococcus ³ 20~30% ƒ w, Staphylococcus, Bacillus, Corynebacterium šwš (10). s k, Micrococcus, Kocuria, Staphylococcus k, Bacillus 90% k y, Pseudomonas 80%, Aeromonas 40% xw (12). wr ü, (2) Staphylococcus 73%, Micrococcus 21%, Lactobacillus 5% š, (3) Staphylococcus 58%, Micrococcus 21%, Enterococcus 10%, Bacillus 7% š wš, Micrococcus ƒ w ü š. w œ» ³ Cladosporium, Aspergillus, Penicillium xw 69% w š, Cladosporium 38% ƒ. Áš w s w œ» ³ w w, 3 77%, Cladosporium 48% w (1). Aspergillus Penicillium w ³ w w, ³ citrinin, gliotoxin, patulin A. versicolorƒ sterigmatocystein (6, 11). w 1 w Stachybotrys p w v ƒ, Stachybotrys S. chartarum ü y ³, satratoxin G, satratoxin H sww ³ w (6). 1,717 r, ƒ ³ Cladosporium, Penicillium, Aspergillus, ü ƒƒ 86%, 80%, 62% y š, ƒ ƒ 40 CFU/m 3, 30 CFU/m 3, 20 CFU/m 3, ƒƒ 92%, 77%, 49%, ƒƒ 200 CFU/m 3, 50 CFU/m 3, 20 CFU/m 3 ùkù, Cladosporium ƒ sw ³ (24). œ» Stachybotrys chartarum ü w 6%, 1% y (24). yl w, üœ» ƒ» Penicillium w, Cladosporium ùkû (16). ³, mw, s û xk p» w w. w Aspergillus, Penicillium, Stachybotrys ƒ sw Cladosporium w xk,, w ³, œ» ³ ³ w ƒ v w š q. w ù ü t w k, ƒ w ³ l œ» w ü t w w y w v. w w w. š x 1., ½ù, ½, ½. 2005. w üy œ» s p. wz 41, 188-194. 2. z, û. 1998. ü œ» w. w wz 8, 231-241. 3. x, y, ½ z, ½x. 2000. w ü œ» sƒ. w wz 10, 115-125. 4. yÿy,, x, ½. 2003. e üy œ» y. wz 39, 253-259. 5. Atlas, R.M. and L.C. Parks. 1996. Handbook of microbiological media. CRC press, Boca Raton, Florida, USA. 6. Brasel, T.L., J.M. Martin, C.G. Carriker, S.C. Wilson, and D.C. Straus. 2005. Detection of airborne Stachybotrys chartarum macrocyclic trichothecene mycotoxins in the indoor environment. Appl. Environ. Microbiol. 71, 7376-7388. 7. Burge, H.A., D.L. Pierson, T.O. Groves, K.F. Strawn, and S.K. Mishra. 2000. Dynamics of airborne fungal populations in a large office building. Curr. Microbiol. 40, 10-16. 8. Cooley, J.D., W.C. Wong, C.A. Jumper, and D.C. Straus. 1998. Correlation between the prevalence of certain fungi and sick building syndrome. Occup. Environ. Med. 55, 579-584. 9. Daisey, J.M., W.J. Angell, and M.G. Apte. 2003. Indoor air quality, ventilation and health symptoms in schools: an analysis of existing information. Indoor Air 13, 53-64. 10. Fang, Z., Z. Ouyang, H. Zheng, X. Wang, and L. Hu. 2007. Culturable airborne bacteria in outdoor environments in Beijing, China. Microb. Ecol. (in press). 11. Fischer, G. and D. Wolfgang. 2003. Relevance of airborne fungi
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(Received June 22, 2007/Accepted September 11, 2007) ABSTRACT : Isolation and Characterization of Airborne Bacteria and Fungi in Indoor Environment of Elementary Schools Na Yeong Kim 1, Young Ran Kim 1, Min Kyu Kim 2, Du Wan Cho 2, and Jongseol Kim 1,2 * ( 1 Graduate School of Education and 2 Department of Biological Science, University of Ulsan, Ulsan 680-749, Korea) Indoor airborne bacterial and fungal concentrations were examined at classrooms and corridors of 3 elementary schools in Ulsan. Airborne microorganisms were collected with an impaction-type air sampler using plate count agar and dichloran rose bengal chloramphenicol agar. During the semester, concentrations of bacteria ranged 168~3,887 MPN/m 3 at classrooms and 168~6,339 MPN/m 3 at corridors, while those of fungi ranged 34~389 MPN/m 3 at classrooms and 91~507 MPN/m 3 at corridors. The bacterial concentrations showed larger variations between situations and schools compared to those of fungi. When airborne bacteria were isolated and identified, 84% were observed as Gram-positive, and Micrococcus spp. was the most abundant group with 61% of tested isolates, followed by genus Staphylococcus with 10%. The Micrococcus spp. isolates, of which 75% were identified as M. luteus, appeared to be from human origins. The protective pigments and substantial cell wall of Micrococcus may provide selective advantage for their survival in the air. We also isolated and identified 15 genera of filamentous fungi. The most common culturable fungi were Cladosporium, Aspergillus and Penicillium, and these 3 genera were 69% of fungal isolates. Genus Stachybotrys, of which S. chartarum is a well known producer of many potent mycotoxins, was also detected from one of the schools. Further systematic studies are necessary with an emphasis on species identification and mycotoxin production of isolated fungal genera, including Aspergillus, Penicillium, and Stachybotrys.