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Bacterial Flora of the Biofilm Formed on the Submerged Surface of the Reed Phragmites Australis

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Bacterial Flora of the Biofilm Formed on the Submerged Surface of the Reed Phragmites Australis Microbes Environ. Vol. 20, No. 1, 14–24, 2005 http://wwwsoc.nii.ac.jp/jsme2/ Bacterial Flora of the Biofilm Formed on the Submerged Surface of the Reed Phragmites australis MASAYASU YAMAMOTO1, HIROSHI MURAI1, AYA TAKEDA1, SUGURU OKUNISHI1 and HISAO MORISAKI1* 1 Faculty of Science and Engineering, Ritsumeikan University, 1–1–1 Noji-higashi, Kusatsu 525–8577, Japan (Received August 31, 2004—Accepted November 8, 2004) Bacterial flora of a biofilm formed on the submerged stems of reeds (Phragmites australis) was studied in comparison with the flora in the water surrounding the reeds and on the aerial stems of the reeds. Most of the iso- lates from the above three samples were Gram-negative (90%) and rod-shaped (87%) with a distinct difference in glucose metabolism: largely oxidative (aerial stem surface), less oxidative (biofilm) and not at all (water). Most of the isolates (90%) belonged to the , , and -Proteobacteria, with Sphingomonadaceae a common group. Isolates from the aerial stem were phylogenetically different from those of the biofilm and water. The bio- film and water samples consisted of a phylogenetically common and a different group. The biofilm was charac- terized by 1) a seasonal change in thickness with a maximum in spring and a minimum in winter, 2) the existence of plastic-degrading strains phylogenetically close to Roseateles depolymerans, and 3) strong denitrifying activi- ty even under aerobic conditions in a thicker biofilm formed in spring. Key words: biofilm, reed surface, bacterial flora, phylogenetic analysis, denitrification activity Reeds (Phragmites australis) are an emergent aquatic ing agent, acting to remove pollutants in the reed belt. macrophyte in wetlands, usually forming homogenous belts In the present study, we report that the bacterial flora of around freshwater lakes. There have been several studies on the reed biofilm is characteristically different from those of the role of wetland plants including reeds in the removal of the aerial surface and the water sample. The denitrifying po- various kinds of pollutants from wastewater6,7,13,18). Howev- tential of the biofilm and the unexpected finding that there er, little study has been done on the microorganisms associ- are plastic-degrading bacterial strains in the biofilm are re- ated with these plants. ported here for the first time. Biofilms, which consist of various microorganisms, have been recognized as a type of microbial community that in- Materials and Methods cludes complex microenvironments differing in the concen- trations of various ions, gases, or nutrients with a thickness Sampling in the order of microns ( ms)4,5). A biofilm can be observed Lake Biwa is the largest lake in Japan (670.29 km2, 41.2 on the submerged surface of a reed. However, there have m deep on average). The reed sample used in this study been no studies as yet of the biofilm formed on the surface (Phragmites australis) was taken from a reed belt (35L19' of reeds. Thus, we aimed to clarify the bacterial flora of the N, 136L04' E) located in the northern basin of Lake Biwa. biofilm and the physiological features of isolates from the The biofilm samples were obtained from the submerged biofilm, making comparisons with the aerial surface of the part (10 to 20 cm under the water) of the stem. The sub- reed and a water sample taken nearby. Secondly, we aimed merged part and the part of exposed to air (10 to 20 cm to investigate the possible role of the biofilm as a denitrify- above the water level) cut from 5 reeds were placed into a sterilized bottle in a cooling box (4LC), brought back to our * Corresponding author; E-mail: [email protected], Tel: laboratory within several hours, and kept in a refrigerator at 81–77–566–2767, Fax: 81–77–561–2659 4LC. The experiments were carried out within the day. A Bacteria in a Reed Biofilm 15 300-ml water sample taken near the sampled reed (ca. 1 m through a Millipore membrane filter (0.20 m); the water away) was also brought back. sample taken from near the reed was also treated. Particles showing a bright blue fluorescence were counted as mi- Measurement of biofilm thickness crobes. The reed sample was sliced (perpendicularly to the reed’s long axis) with a razor to obtain a thin disk (ca. less than Isolation of microbes 100 m thick); 2 slices were made from each reed sample. The samples were collected on September 6, 1999. In The thickness of the biofilm formed around the thin disk Lake Biwa, the water level usually changes within a range was observed at three different positions on a photograph of ca. 1 m through the year (maximum in spring and mini- taken using an Olympus model BX-50 phase-contrast mi- mum in winter), but is rather stable in autumn. This was croscope (magnificationP400): From the photograph, the also the case in the year 1999: From early in July to the mid- thickness was determined by measuring the distance from dle of October the difference in the water level remained the outermost surface of the reed carrying a biofilm to the within ca. 10 cm. In autumn, the reeds reach a height of boundary between the biofilm and the surface of the stem around 3 m before withering during the late autumn and which was easily distinguished from the outer biofilm. The winter. Because of the stable water level and stable appear- average of these thicknesses for 4 different reeds in good ance of the reeds, the biofilm was expected to be most stable condition out of 5 sampled reeds was defined as the reed’s in autumn in terms of characteristics such as bacterial flora biofilm thickness. Thus, the average value was obtained and function. The biofilm and the aerial surface were wiped from 24 positions, i.e., 4 (reeds)P2 (slices/reed)P3 (posi- carefully with cotton and the cotton was treated as described tions/slice). above (see Total number of microbes). The water sample was then serially diluted 102–104-fold in sterilized water. Measurement of wet weight of biofilm DNB agar (1.5 wt%) medium was mixed with the diluted The biofilm on the submerged part of the reed was re- samples; the water sample taken from near the reeds was moved with a toothbrush in distilled water until a fresh reed also treated. The DNB medium was a 100-fold dilution of surface appeared. Then, the suspension was filtered through the NB medium that contained (per liter), 10 g of Nihon a Whatman GF/F Glass Microfibre Filter until no excess Seiyaku polypeptone, 10 g of Wako Pure Chemicals bonito water remained. The weight of the wet biofilm was mea- extract, and 5 g of NaCl (pH 7.2). The plates were incubated sured with a Sartorius model BP121S balance as the in- aerobically at 20LC for 30 days, with the number of new crease in the weight of the filter after the filtration of the colonies appearing counted every day. The colonies were biofilm sample. This weight was divided by the surface area distinguished by marking each colony from the back of the of the reed from which the biofilm was removed to obtain Petri dish with a pen of different color and different shape the wet weight of the biofilm per unit surface. each day. After the incubation period, the strains were ran- domly isolated from the colonies. Total number of microbes The total number of microbes in each sample was count- Morphological and physiological traits of isolates ed under an Olympus model BX50 BX-FLA epifluores- The isolated strains were characterized by examining cence microscope using the following method. The sub- morphological and physiological traits. The cell size and merged surface where the biofilm was formed and the Gram staining reaction were examined for the cells incubat- surface exposed to air (hereafter referred to as the “aerial ed for 1–2 days in DNB liquid medium at 100 rpm and stem surface”) were wiped carefully with sterilized cotton. 20LC. Each colony’s size, its color, and the roughness of the Each cotton wad was put into its own sterilized plastic bot- colony’s edge were also examined after 2–7 days incubation tle and brought back to the laboratory. The cotton sample, on DNB agar at 20LC. which contained a sample of the biofilm or the aerial stem The isolates were characterized using oxidase, catalase, surface, was placed in 100 ml of sterilized water, and soni- and Oxidation-Fermentation (OF) tests. Some strains were cated with a Branson model 2510JMT ultrasonic cleaner for quite closely related to Roseateles depolymerans, which has 2 min. The samples were diluted in distilled water and fixed been known to degrade plastic15), according to a phylogenet- with glutaraldehyde (final concentration, 1%). The cells ic analysis. So, poly -caprolactone (PCL) degradability were then stained with a DAPI (4',6-diamidino-2-phenylin- was examined as reported previously11). Each isolate was in- dole) solution (final concentration, 1 mg/ml) and filtered oculated onto agar medium containing (per liter) 1 g of 16 YAMAMOTO et al. emulsified PCL (Daicel Chemical Industries, Sakai, Japan), formed. 250 mg of yeast extract, 10 mg of FeSO4·7H2O, 200 mg of Nucleotide sequence accession numbers MgSO4·7H2O, 1000 mg of (NH4)2SO4, 20 mg of CaCl2·2H2O, 0.5 mg of Na2WO4, 0.5 mg of MnSO4, and 100 All the sequences of the 16S rRNA gene determined in mg of surface-active agent Plysurf A 210G (Daiichi Kogyo this study have been submitted to DDBJ under the accession Seiyaku, Kyoto, Japan) in 10.7 mM KH2PO4/K2HPO4 (pH numbers AB097959 to AB098021.
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