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Divergent Nod-Containing Bradyrhizobium Sp. DOA9 with a Megaplasmid and Its Host Range

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Divergent Nod-Containing Bradyrhizobium Sp. DOA9 with a Megaplasmid and Its Host Range Divergent Nod-Containing Bradyrhizobium sp. DOA9 with a Megaplasmid and its Host Range KamonlucK TeamTisong1, PongPan songwaTTana2, RujiReK noisangiam2, PongdeT PiRomyou2, nanTaKoRn BoonKeRd2, Panlada TiTTaBuTR2, Kiwamu minamisawa3, achaRa nanTagij4, shin oKazaKi5, miKiKo aBe6, ToshiKi uchiumi6*, and neung TeaumRoong2** 1&HQWHUIRU6FLHQWL¿FDQG7HFKQRORJLFDO(TXLSPHQW6XUDQDUHH8QLYHUVLW\RI7HFKQRORJ\0XDQJ1DNKRQ5DWFKDVLPD7KDLODQG 26FKRRORI%LRWHFKQRORJ\6XUDQDUHH8QLYHUVLW\RI7HFKQRORJ\0XDQJ1DNKRQ5DWFKDVLPD7KDLODQG3*UDGXDWH6FKRRORI/LIH 6FLHQFH7RKRNX8QLYHUVLW\6HQGDL-DSDQ46RLO0LFURELRORJ\*URXS'LYLVLRQRI6RLO6FLHQFH'HSDUWPHQWRI$JULFXOWXUH %DQJNRN7KDLODQG5*UDGXDWH6FKRRORI$JULFXOWXUH7RN\R8QLYHUVLW\RI$JULFXOWXUHDQG7HFKQRORJ\7RN\R-DSDQDQG 6*UDGXDWH6FKRRORI6FLHQFHDQG(QJLQHHULQJ.DJRVKLPD8QLYHUVLW\.DJRVKLPD-DSDQ (Received May 13, 2014—Accepted August 15, 2014—Published online October 4, 2014) %UDG\UKL]RELXP sp. DOA9, a non-photosynthetic bacterial strain originally isolated from the root nodules of the legume $HVFK\QRPHQHDPHULFDQD, is a divergent QRGFRQWDLQLQJVWUDLQ,WH[KLELWVDEURDGKRVWUDQJHEHLQJDEOHWRFRORQL]HDQGHI¿- ciently nodulate the roots of most plants from the Dalbergioid, Millettioid, and Robinioid tribes (7 species of Papilionoideae). In all cases, nodulation was determinate. The morphology and size of DOA9 bacteroids isolated from the nodules of various species of Papilionoideae were indistinguishable from the free-living form. However, they were spherical in $UDFKLVK\SRJDHD nodules. GusA-tagged DOA9 also colonized rice roots as endophytes. Since broad-host-range legume symbionts often carry multiple replicons in their genome, we analyzed the replicons for symbiosis genes by electrophoresis. DOA9 carried two replicons, a chromosome (cDOA9) and single megaplasmid (pDOA9) larger than 352 kb. The genes for nodulation (QRG$, %, C DQGQLWURJHQ¿[DWLRQ nifH) were localized on the megaplasmid. Southern blot hybridization revealed two copies of QRG$ on the megaplasmid, single copies of QRG% and C on the megaplasmid, and one copy each of nifH on the chromosome and megaplasmid. These results suggested that %UDG\UKL]RELXP sp. DOA9 may have the unusual combination of a broad host range, bacteroid differentiation, and symbiosis-mediating replicons. Key words: %UDG\UKL]RELXP, $HVFK\QRPHQHDPHULFDQD, broad host range, megaplasmid The genus $HVFK\QRPHQH belongs to the Dalbergioid clade of the 16S rRNA gene and housekeeping genes (GQD., UHF$, of the subfamily Papilionoideae of the family Fabaceae (19). and JOQ%). DOA9 was called a divergent QRG-containing $HVFK\QRPHQH species establish a symbiotic relationship strain based on Southern blot hybridization with the QRG gene with bacteria of the genus %UDG\UKL]RELXP (19, 27). They (QRG$, %, and C) probes. In addition, on the basis of nifH KDYHEHHQFODVVL¿HGLQWRRQHRIWKUHHFURVVLQRFXODWLRQ &, sequence similarities, DOA9 was placed in a cluster of JURXSV &, JURXS VSHFLHV VXFK DV $ DPHULFDQD and $ QRQSKRWRV\QWKHWLFEUDG\UKL]RELDOVWUDLQVWKDWDUHDEOHWR¿[ HODSKUR[\ORQ, are only nodulated on their roots by non- nitrogen in the free-living form. Moreover, it can nodulate a SKRWRV\QWKHWLFEUDG\UKL]RELD&,JURXSVSHFLHVVXFKDV$ wide range of legumes, including 0DFURSWLOLXPDWURSXUSXUHXP, DIUDVSHUD and $ QLORWLFD, are nodulated on their roots and $UDFKLVK\SRJDHD, 9LJQDUDGLDWD, and $HVFK\QRPHQHDIUDVSHUD stems by both non-photosynthetic and photosynthetic (29). Since information regarding this strain is limited, we EUDG\UKL]RELD&,JURXSVSHFLHVVXFKDV$LQGLFD and $ investigated the root colonization, infection, and nodulation VHQVLWLYD, are nodulated on their roots and stems by photosyn- HI¿FLHQF\ RI '2$ LQ VHYHUDO VSHFLHV IURP WKH OHJXPH WKHWLF EUDG\UKL]RELD &, JURXS VSHFLHV DUH QRGXODWHG E\ subfamilies Papilionoideae and Mimosoideae, as well as rice. strains BTAi1 and ORS278 in a Nod factor–independent We also examined bacteroids and nodule development. manner (27). However, $LQGLFD &,JURXS ZDVUHFHQWO\ Previous studies demonstrated that symbionts with a broad found to be nodulated by a non-photosynthetic strain isolated host range generally carried multiple replicons in their from $DPHULFDQD &,JURXS 7KLVVWUDLQFRXOGQRGXODWH genome (12, 36, 42); therefore, we examined the replicon VHYHUDO&,JURXSVRI$HVFK\QRPHQH, as well as the peanut and structure, localization, and copy number of symbiosis genes. mung bean (29). %UDG\UKL]RELXP sp. DOA9 (Alphaproteobacteria) was Materials and Methods isolated from the root nodules of $DPHULFDQD in Thailand. This strain was assigned to % \XDQPLQJHQVH based on its %DFWHULDOVWUDLQVDQGJURZWKFRQGLWLRQV phenotypic characteristics and multilocus sequences analysis %UDG\UKL]RELXP sp. DOA9, % GLD]RHI¿FLHQV USDA110, and 0HVRUKL]RELXP ORWL 0$)) ZHUH FXOWXUHG DW & LQ +0 medium supplemented with l-arabinose (8). GUS-tagged DOA9 was &RUUHVSRQGLQJDXWKRU(PDLOXWWDQ#VFLNDJRVKLPDXDFMS cultured in HM supplemented with streptomycin (200 Pg mL1) (29). Tel: 81–99–285–8164; Fax: 81–99–285–8163. &RUUHVSRQGLQJDXWKRU(PDLOQHXQJ#VXWDFWK 3ODQWJURZWKDQGLQRFXODWLRQ Tel: 66–44–223350; Fax: 66–44–216345. Peanut ($UDFKLVK\SRJDHD), mung bean (9LJQDUDGLDWD), soybean Reproduced from Microbes Environ. 29: 370-376 (2014). Kamonluck Teamtisong: Participant of the 30th UM, 2002-2003. 291 291 (*O\FLQH PD[ cv. SJ5), siratro (0DFURSWLOLXP DWURSXUSXUHXP), &HOOSHOOHWVZHUHKDUYHVWHGE\FHQWULIXJDWLRQDWîJ for 10 min. 6HVEDQLDURVWUDWD, lupin (/XSLQXVSRO\SK\OOXV), 'HVPRGLXP sp., alfalfa 7KHFHOOVZHUHUHVXVSHQGHGLQ ZY 1D&OWR2'600 1. They (0HGLFDJR VDWLYD), 0HGLFDJR WUXQFDWXOD, and $FDFLD PDQJLXP were harvested from 1 mL of a cell suspension and washed with seeds were sterilized as described previously (37). $HVFK\QRPHQH 0 VDOWV FRQWDLQLQJ 0 1D&O DQG WKHQ ZLWK P/ DPHULFDQD (a local Thai variety), $DIUDVSHUD, $HYHQLD (provided by (w/v) Sarcosyl. The supernatant was removed immediately and the (ULF*LUDXG DQG$LQGLFD (ecotype Tottori, Japan; ecotype Tomeshi, sediment was resuspended in 50 PL of lysis buffer (1 mg mLí Japan; and a local Thai variety) were sterilized by incubating in lysozyme, 1 mg mLí RNase A [33], 0.1% (w/v) bromophenol blue concentrated sulfuric acid for 30 min. The seeds of ,QGLJRIHUD in Trisborate buffer (pH 8.2, 89 mM Tris base, 12.5 mM disodium WLQFWRULD, /RWXVMDSRQLFXV, 6W\ORVDQWKHVKDPDWD, &URWDODULDMXQFHD, ('7$DQGP0ERULFDFLG>@DQG>YY@JO\FHURO /HVSHGH]D sp., /HXFDHQDOHXFRFHSKDOD, 0LPRVDSXGLFD, 1HSWXQLD Before sample loading, electrophoresis was performed on a QDWDQV, and 6DPDQHDVDPDQ were sterilized by incubating in con- DJDURVH JHO ZKLFK OHYHOHG RII ZLWK î7%( EXIIHU & centrated sulfuric acid for 10 min. The seeds of rice (2U\]DVDWLYD XQWLO LW WRXFKHG WKH JHO 7KH ZHOOV ZHUH WKHQ ¿OOHG ZLWK PL ssp. LQGLFD) were sterilized as described previously (26). All seeds Sodium Dodecyl Sulfate (SDS; 10% [w/v]) mixed with xylene cyanol were washed with sterilized water and then soaked in sterilized (1 mg mL1). The current was run for 10–15 min at 100 V with water overnight at ambient temperature. All seeds were germinated reversed polarity until SDS was 1 cm above the wells. After that, RQVWHULOL]HG ZY ZDWHUDJDUIRUWRGDW&LQWKHGDUN 50 PL of sample mixed with lysis buffer was directly loaded The germinated seeds were transferred onto Hoagland’s agar (15). and left for 15 min before 15 PL of Proteinase K (5 mg mL1) in %UDG\UKL]RELXP VS '2$ ZDV ZDVKHG ZLWK 1D&O DQG 40% (w/v) glycerol was overlaid. The wells were sealed with melted optical density at 600 nm (OD600 ZDVDGMXVWHGWRZLWKVWHULOL]HG DJDURVHJHODQGî7%(EXIIHUZDVWKHQDGGHGWRFRYHUWKHJHO water, corresponding to approximately 109 cells mL1(DFKVHHG- After 1 h, electrophoresis was carried out in a cold chamber at ling was then inoculated with 100 PL of the bacterial culture. All &7KHFXUUHQWZDVUXQDWP$IRUKDQGDWP$IRUD SODQWVZHUHJURZQDW&XQGHUDKOLJKWKGDUNF\FOHDWDOLJKW further 10 h. The DNA in the gel was stained for 30 min in ethidium intensity of 639 P(P2 s1 for 7 to 14 d (43). These samples were bromide (0.5 Pg mL1) and washed with distilled water before being used for microscopic observations. The symbiotic abilities of DOA9 viewed under UV light. ZHUHGHWHUPLQHGLQ/HRQDUG¶VMDUVFRQWDLQLQJVWHULOL]HGYHUPLFXOLWH and inoculated with 1 mL of bacterial culture, as described above. 6RXWKHUQEORWK\EULGL]DWLRQ 1IUHH+RDJODQG¶VVROXWLRQZDVDGGHGWRHDFKMDUDVUHTXLUHG3ODQWV The megaplasmid and chromosomal DNAs separated on the were harvested after 35 d, used in an analysis of nitrogenase activity gel were used for the Southern blot hybridization of nodulation by the Acetylene Reduction Assay, and the number of nodules was (QRG DQGQLWURJHQ¿[DWLRQ nifH JHQHVDVGHVFULEHG %ULHÀ\ scored. The dry weights of plants were determined after drying at probes for QRG$ (550 bp), QRG% (530 bp), and QRG& (1 kb) were &IRUK REWDLQHG WKURXJK 3&5 DPSOL¿FDWLRQ XVLQJ WKH JHQRPLF '1$ RI % \XDQPLQJHQVH SUTN6-2, % FDQDULHQVH SUTN7-2, and % 0LFURVFRSLFREVHUYDWLRQRIURRWFRORQL]DWLRQDQGQRGXODWLRQ GLD]RHI¿FLHQV USDA110, respectively. DNA fragments of the Root colonization and nodulation were revealed by GUS staining. UHVSHFWLYHVWUDLQVZHUHDPSOL¿HGZLWKWKHSULPHUSDLUVQRG$<) Samples inoculated with GUS-tagged DOA9 were immersed in QRG$<5 QRG$), nodB26/nodB625 (QRG% DQG QRG& GUS assay solution (40 mL 20 mg mL1 X-Gluc in 11-dimethyl- QRG&, QRG&) (29). The probe for nifH was derived from % formamide, 20 mg SDS, 2 mL methanol, 0.2 mL 1 M sodium phos- \XDQPLQJHQVH using nifHF/nifHI primer pairs (18). DNA probes phate buffer, and 7.76 mL distilled water) in a vacuum for 120 min ZHUHODEHOHGRYHUQLJKWDW&E\UDQGRPSULPLQJDQGK\EULGL]HG DQGOHIWLQWKLVVROXWLRQIRUKDW&*86VWDLQLQJZDVREVHUYHG
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