Identification of direct transcriptional target genes of ExoS/ChvI two-component signaling in Sinorhizobium meliloti
The Sinorhizobium meliloti ExoS/ChvI two-component signaling pathway is required for the development of a nitrogen-fixing symbiosis between S. meliloti and its plant hosts. ExoS/ChvI also has important roles in regulating succinoglycan production, biofilm formation, motility, nutrient utilization, a...
Saved in:
| Published in: | Journal of bacteriology Vol. 191; no. 22; pp. 6833 - 6842 |
|---|---|
| Main Authors: | , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
01.11.2009
|
| Subjects: | |
| ISSN: | 1098-5530 |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | The Sinorhizobium meliloti ExoS/ChvI two-component signaling pathway is required for the development of a nitrogen-fixing symbiosis between S. meliloti and its plant hosts. ExoS/ChvI also has important roles in regulating succinoglycan production, biofilm formation, motility, nutrient utilization, and the viability of free-living bacteria. Previous microarray experiments with an exoS96::Tn5 mutant indicated that ExoS/ChvI influences the expression of a few hundred genes, complicating the investigation of which downstream genes respond directly or indirectly to ExoS/ChvI regulation. To focus our study of ExoS/ChvI transcriptional target genes, we performed transcriptional profiling with chvI gain-of-function and reduced-function strains. The chvI gain-of-function strain that we used contains a dominant gain-of-function chvI allele in addition to wild-type chvI. We identified genes that, relative to their expression level in the wild type, are both upregulated in the chvI gain-of-function strain and downregulated in the reduced-function strain or vice versa. Guided by this focused set of genes, we performed gel mobility shift assays and demonstrated that ChvI directly binds the intergenic regions upstream of ropB1, SMb21440, and SMc01580. Furthermore, DNase I footprint analysis of the region upstream of SMc01580 identified a specific DNA sequence bound by ChvI and allowed the discovery of a possible motif for ChvI binding. Our results provide insight into the mechanism of how ExoS/ChvI regulates its downstream targets and lay a foundation for studying this conserved pathway with critical roles in free-living and symbiotic bacteria. |
|---|---|
| AbstractList | The Sinorhizobium meliloti ExoS/ChvI two-component signaling pathway is required for the development of a nitrogen-fixing symbiosis between S. meliloti and its plant hosts. ExoS/ChvI also has important roles in regulating succinoglycan production, biofilm formation, motility, nutrient utilization, and the viability of free-living bacteria. Previous microarray experiments with an exoS96::Tn5 mutant indicated that ExoS/ChvI influences the expression of a few hundred genes, complicating the investigation of which downstream genes respond directly or indirectly to ExoS/ChvI regulation. To focus our study of ExoS/ChvI transcriptional target genes, we performed transcriptional profiling with chvI gain-of-function and reduced-function strains. The chvI gain-of-function strain that we used contains a dominant gain-of-function chvI allele in addition to wild-type chvI. We identified genes that, relative to their expression level in the wild type, are both upregulated in the chvI gain-of-function strain and downregulated in the reduced-function strain or vice versa. Guided by this focused set of genes, we performed gel mobility shift assays and demonstrated that ChvI directly binds the intergenic regions upstream of ropB1, SMb21440, and SMc01580. Furthermore, DNase I footprint analysis of the region upstream of SMc01580 identified a specific DNA sequence bound by ChvI and allowed the discovery of a possible motif for ChvI binding. Our results provide insight into the mechanism of how ExoS/ChvI regulates its downstream targets and lay a foundation for studying this conserved pathway with critical roles in free-living and symbiotic bacteria. |
| Author | Perovich, Virginia M Chen, Esther J Fisher, Robert F Sabio, Erich A Long, Sharon R |
| Author_xml | – sequence: 1 givenname: Esther J surname: Chen fullname: Chen, Esther J email: echen@fullerton.edu organization: Department of Biological Science, Center for Applied Biotechnology Studies, College of Natural Sciences and Mathematics, California State University Fullerton, 800 N. State College Blvd., Fullerton, CA 92834-6850, USA. echen@fullerton.edu – sequence: 2 givenname: Robert F surname: Fisher fullname: Fisher, Robert F – sequence: 3 givenname: Virginia M surname: Perovich fullname: Perovich, Virginia M – sequence: 4 givenname: Erich A surname: Sabio fullname: Sabio, Erich A – sequence: 5 givenname: Sharon R surname: Long fullname: Long, Sharon R |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19749054$$D View this record in MEDLINE/PubMed |
| BookMark | eNo1kLtPwzAYxC0Eog-Y2JEntrSf4ziPEaoCRZUYCnPkOHZqlNjBdnj99aSiTCedfjrd3QydGmskQlcEFoTE-fLpbgGQ0SSC4gRNCRR5xBiFCZp5_wZAkoTF52hCiiwpgCVTFDa1NEErLXjQ1mCrcK2dFAEHx40XTvcHn7c4cNfIgBtppD9g6y-7W672HxscPm0kbNePVUzAXjcjrk2DtcE7bazb6x9b6aHDnWx1a4O-QGeKt15eHnWOXu_XL6vHaPv8sFndbiORpFmIVFFnIiecSkmqhOaJSlPFmKghBpoWfBzK8orGhEpV5awmtYiVAKCQcwJQxXN085fbO_s-SB_KTnsh25YbaQdfpmlKxyfoCF4fwaHqZF32TnfcfZf_P8W_rwxrLQ |
| CitedBy_id | crossref_primary_10_1111_j_1365_294X_2012_05629_x crossref_primary_10_1128_JB_00199_21 crossref_primary_10_1128_JB_01751_14 crossref_primary_10_1093_femsre_fuac048 crossref_primary_10_3390_ijms22126233 crossref_primary_10_1111_j_1574_6968_2012_02645_x crossref_primary_10_1128_JB_06357_11 crossref_primary_10_3389_fpls_2021_678976 crossref_primary_10_1073_pnas_1400450111 crossref_primary_10_1128_JB_00501_17 crossref_primary_10_1094_MPMI_12_14_0407_R crossref_primary_10_3389_fmicb_2023_1241143 crossref_primary_10_3389_fmicb_2022_1020932 crossref_primary_10_1111_mmi_14823 crossref_primary_10_3390_agronomy15051235 crossref_primary_10_1094_MPMI_09_13_0284_R crossref_primary_10_1128_JB_05371_11 crossref_primary_10_1186_1471_2180_13_132 crossref_primary_10_1371_journal_pone_0135655 crossref_primary_10_1016_j_carbpol_2025_124010 crossref_primary_10_1093_femsle_fnx061 crossref_primary_10_3389_fpls_2014_00730 crossref_primary_10_1073_pnas_1917471117 crossref_primary_10_1128_JB_02626_14 crossref_primary_10_1128_mSystems_00035_17 crossref_primary_10_1091_mbc_E24_12_0546 crossref_primary_10_1371_journal_pgen_1010776 crossref_primary_10_1146_annurev_micro_120822_102714 crossref_primary_10_1073_pnas_1610724113 crossref_primary_10_1128_JB_01456_10 crossref_primary_10_1007_s11306_017_1210_2 crossref_primary_10_1128_JB_01676_09 crossref_primary_10_1128_JB_00665_17 crossref_primary_10_1007_s42994_024_00193_1 crossref_primary_10_1016_j_micpath_2023_106442 crossref_primary_10_1111_mmi_14119 crossref_primary_10_1128_jb_00182_25 |
| ContentType | Journal Article |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1128/JB.00734-09 |
| DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic MEDLINE |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Biology |
| EISSN | 1098-5530 |
| EndPage | 6842 |
| ExternalDocumentID | 19749054 |
| Genre | Research Support, U.S. Gov't, Non-P.H.S Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural |
| GrantInformation_xml | – fundername: NIGMS NIH HHS grantid: R01-GM30692 |
| GroupedDBID | --- -DZ -~X .55 .GJ 0R~ 186 18M 1VV 29J 2WC 39C 3O- 4.4 53G 5GY 5RE 5VS 79B 85S 8WZ 9M8 A6W AAGFI ABPPZ ACGFO ACGOD ACNCT ACPRK ADBBV ADXHL AENEX AFFDN AFFNX AFRAH AGCDD AGVNZ AI. AIDAL AJUXI ALMA_UNASSIGNED_HOLDINGS AOIJS BAWUL BKOMP BTFSW C1A CGR CJ0 CS3 CUY CVF DIK DU5 E3Z EBS ECM EIF EJD F5P FRP GX1 H13 HYE HZ~ IH2 KQ8 L7B MVM NHB NPM O9- OHT OK1 P-O P-S P2P PQQKQ QZG RHI RNS RPM RSF RXW TAE TR2 UHB UKR UPT VH1 W8F WH7 WHG WOQ X7M Y6R YQT YR2 YZZ ZCA ZCG ZGI ZXP ZY4 ~02 ~KM 7X8 |
| ID | FETCH-LOGICAL-c467t-f9d7c81a3ee1b4384f66f55cd020369a07358b3213efb85d1dc2fc00308a100b2 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 43 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000271195300009&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| IngestDate | Wed Oct 01 15:09:09 EDT 2025 Mon Jul 21 05:59:29 EDT 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 22 |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c467t-f9d7c81a3ee1b4384f66f55cd020369a07358b3213efb85d1dc2fc00308a100b2 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/2772461 |
| PMID | 19749054 |
| PQID | 66639743 |
| PQPubID | 23479 |
| PageCount | 10 |
| ParticipantIDs | proquest_miscellaneous_66639743 pubmed_primary_19749054 |
| PublicationCentury | 2000 |
| PublicationDate | 2009-11-00 |
| PublicationDateYYYYMMDD | 2009-11-01 |
| PublicationDate_xml | – month: 11 year: 2009 text: 2009-11-00 |
| PublicationDecade | 2000 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Journal of bacteriology |
| PublicationTitleAlternate | J Bacteriol |
| PublicationYear | 2009 |
| References | 2793828 - J Bacteriol. 1989 Oct;171(10):5492-502 18284576 - Mol Microbiol. 2008 Mar;67(6):1292-306 8325480 - Genetics. 1993 Jun;134(2):435-44 8144468 - J Bacteriol. 1994 Apr;176(7):1997-2002 16629750 - FEMS Microbiol Ecol. 2006 May;56(2):195-206 10542182 - J Bacteriol. 1999 Nov;181(21):6788-96 8710923 - Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8636-41 7635814 - J Bacteriol. 1995 Aug;177(15):4289-96 8331671 - J Mol Biol. 1993 Jul 5;232(1):67-78 6330025 - J Bacteriol. 1984 Jul;159(1):125-9 11474104 - Science. 2001 Jul 27;293(5530):668-72 16735738 - Microbiology. 2006 Jun;152(Pt 6):1751-63 15342573 - J Bacteriol. 2004 Sep;186(18):6042-9 9802033 - Microbiology. 1998 Oct;144 ( Pt 10):2915-24 10948423 - Biotechniques. 2000 Aug;29(2):240-2, 244-5 10361286 - Mol Microbiol. 1999 May;32(4):837-49 8589411 - Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):549-59 16816173 - J Bacteriol. 2006 Jul;188(14):5003-13 18631237 - Mol Microbiol. 2008 Sep;69(5):1290-303 3013840 - J Bacteriol. 1986 Jul;167(1):66-72 15542588 - Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16636-41 14769477 - FEMS Microbiol Lett. 2004 Feb 9;231(1):131-6 12813079 - J Bacteriol. 2003 Jul;185(13):3853-62 18375818 - Microbiology. 2008 Apr;154(Pt 4):1258-70 7559334 - J Bacteriol. 1995 Oct;177(19):5485-94 15263816 - J Mol Microbiol Biotechnol. 2004;7(3):115-32 12653992 - Eur J Biochem. 2003 Apr;270(7):1365-80 16980496 - J Bacteriol. 2006 Oct;188(19):6932-42 15205418 - J Bacteriol. 2004 Jul;186(13):4168-76 9701808 - Mol Microbiol. 1998 Jul;29(1):125-38 11497462 - Mol Plant Microbe Interact. 2001 Aug;14(8):1016-25 17462014 - Mol Microbiol. 2007 May;64(3):647-64 3862129 - Proc Natl Acad Sci U S A. 1985 Sep;82(18):6231-5 15292148 - J Bacteriol. 2004 Aug;186(16):5460-72 9748453 - J Bacteriol. 1998 Oct;180(19):5183-91 9422587 - J Bacteriol. 1998 Jan;180(1):20-6 6274841 - J Bacteriol. 1982 Jan;149(1):114-22 7873780 - Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):758-65 17632573 - Nat Rev Microbiol. 2007 Aug;5(8):619-33 18842098 - Mol Plant Microbe Interact. 2008 Nov;21(11):1498-509 17158704 - Microbiol Mol Biol Rev. 2006 Dec;70(4):910-38 11918800 - Mol Microbiol. 2002 Mar;43(5):1115-27 8407839 - J Bacteriol. 1993 Oct;175(20):6614-25 16535451 - Appl Environ Microbiol. 1996 Nov;62(11):4260-2 15187185 - Microbiol Mol Biol Rev. 2004 Jun;68(2):280-300 18310071 - J Biol Chem. 2008 Apr 18;283(16):10415-24 10485295 - Mol Gen Genet. 1999 Jul;261(6):1032-44 11274120 - J Bacteriol. 2001 Apr;183(8):2595-604 9204561 - Mol Plant Microbe Interact. 1997 Jul;10(5):550-9 11902715 - Mol Microbiol. 1997 Jul;25(1):117-34 2842307 - J Bacteriol. 1988 Sep;170(9):4249-56 12218184 - Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12369-74 10894742 - J Bacteriol. 2000 Aug;182(15):4310-8 3288541 - Genes Dev. 1988 Mar;2(3):282-93 12218183 - Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12375-80 19395488 - J Bacteriol. 2009 Jul;191(13):4372-82 |
| References_xml | – reference: 12218184 - Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12369-74 – reference: 11497462 - Mol Plant Microbe Interact. 2001 Aug;14(8):1016-25 – reference: 3288541 - Genes Dev. 1988 Mar;2(3):282-93 – reference: 10894742 - J Bacteriol. 2000 Aug;182(15):4310-8 – reference: 18842098 - Mol Plant Microbe Interact. 2008 Nov;21(11):1498-509 – reference: 17462014 - Mol Microbiol. 2007 May;64(3):647-64 – reference: 10542182 - J Bacteriol. 1999 Nov;181(21):6788-96 – reference: 8589411 - Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):549-59 – reference: 10361286 - Mol Microbiol. 1999 May;32(4):837-49 – reference: 18310071 - J Biol Chem. 2008 Apr 18;283(16):10415-24 – reference: 15342573 - J Bacteriol. 2004 Sep;186(18):6042-9 – reference: 12218183 - Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12375-80 – reference: 10948423 - Biotechniques. 2000 Aug;29(2):240-2, 244-5 – reference: 15542588 - Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16636-41 – reference: 17158704 - Microbiol Mol Biol Rev. 2006 Dec;70(4):910-38 – reference: 3013840 - J Bacteriol. 1986 Jul;167(1):66-72 – reference: 7873780 - Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):758-65 – reference: 15292148 - J Bacteriol. 2004 Aug;186(16):5460-72 – reference: 12653992 - Eur J Biochem. 2003 Apr;270(7):1365-80 – reference: 16816173 - J Bacteriol. 2006 Jul;188(14):5003-13 – reference: 15205418 - J Bacteriol. 2004 Jul;186(13):4168-76 – reference: 9204561 - Mol Plant Microbe Interact. 1997 Jul;10(5):550-9 – reference: 8710923 - Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8636-41 – reference: 12813079 - J Bacteriol. 2003 Jul;185(13):3853-62 – reference: 9422587 - J Bacteriol. 1998 Jan;180(1):20-6 – reference: 8144468 - J Bacteriol. 1994 Apr;176(7):1997-2002 – reference: 14769477 - FEMS Microbiol Lett. 2004 Feb 9;231(1):131-6 – reference: 9701808 - Mol Microbiol. 1998 Jul;29(1):125-38 – reference: 19395488 - J Bacteriol. 2009 Jul;191(13):4372-82 – reference: 6330025 - J Bacteriol. 1984 Jul;159(1):125-9 – reference: 8407839 - J Bacteriol. 1993 Oct;175(20):6614-25 – reference: 9802033 - Microbiology. 1998 Oct;144 ( Pt 10):2915-24 – reference: 7559334 - J Bacteriol. 1995 Oct;177(19):5485-94 – reference: 8325480 - Genetics. 1993 Jun;134(2):435-44 – reference: 15263816 - J Mol Microbiol Biotechnol. 2004;7(3):115-32 – reference: 11474104 - Science. 2001 Jul 27;293(5530):668-72 – reference: 16735738 - Microbiology. 2006 Jun;152(Pt 6):1751-63 – reference: 18631237 - Mol Microbiol. 2008 Sep;69(5):1290-303 – reference: 18284576 - Mol Microbiol. 2008 Mar;67(6):1292-306 – reference: 11902715 - Mol Microbiol. 1997 Jul;25(1):117-34 – reference: 18375818 - Microbiology. 2008 Apr;154(Pt 4):1258-70 – reference: 8331671 - J Mol Biol. 1993 Jul 5;232(1):67-78 – reference: 2842307 - J Bacteriol. 1988 Sep;170(9):4249-56 – reference: 3862129 - Proc Natl Acad Sci U S A. 1985 Sep;82(18):6231-5 – reference: 16629750 - FEMS Microbiol Ecol. 2006 May;56(2):195-206 – reference: 9748453 - J Bacteriol. 1998 Oct;180(19):5183-91 – reference: 11918800 - Mol Microbiol. 2002 Mar;43(5):1115-27 – reference: 17632573 - Nat Rev Microbiol. 2007 Aug;5(8):619-33 – reference: 16535451 - Appl Environ Microbiol. 1996 Nov;62(11):4260-2 – reference: 10485295 - Mol Gen Genet. 1999 Jul;261(6):1032-44 – reference: 6274841 - J Bacteriol. 1982 Jan;149(1):114-22 – reference: 16980496 - J Bacteriol. 2006 Oct;188(19):6932-42 – reference: 15187185 - Microbiol Mol Biol Rev. 2004 Jun;68(2):280-300 – reference: 11274120 - J Bacteriol. 2001 Apr;183(8):2595-604 – reference: 2793828 - J Bacteriol. 1989 Oct;171(10):5492-502 – reference: 7635814 - J Bacteriol. 1995 Aug;177(15):4289-96 |
| SSID | ssj0014452 |
| Score | 2.162208 |
| Snippet | The Sinorhizobium meliloti ExoS/ChvI two-component signaling pathway is required for the development of a nitrogen-fixing symbiosis between S. meliloti and its... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | 6833 |
| SubjectTerms | Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Proteins - physiology Base Sequence DNA - metabolism DNA Footprinting Electrophoretic Mobility Shift Assay Gene Expression Regulation, Bacterial - genetics Gene Expression Regulation, Bacterial - physiology Molecular Sequence Data Oligonucleotide Array Sequence Analysis Protein Binding Sinorhizobium meliloti - genetics Sinorhizobium meliloti - metabolism Transcription Factors - genetics Transcription Factors - metabolism Transcription Factors - physiology |
| Title | Identification of direct transcriptional target genes of ExoS/ChvI two-component signaling in Sinorhizobium meliloti |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/19749054 https://www.proquest.com/docview/66639743 |
| Volume | 191 |
| WOSCitedRecordID | wos000271195300009&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1LS8NAEF6qVfDi-1Gfe_C6NMlumgQE0WJRwVKoQm9hsw8NtNnaplX_vbN54E0PXnIIu8syO_lmsvPNDEKX8FeVKEcwIhmXhHHHIYmQPmFacdCPgErFimYTQb8fjkbRoIGu6lwYS6usMbEAammEvSNvg5sNppPR6-k7sT2jbGy1aqCxgpoUHBlL6ApGPzEExnyvysgDEG4_3toy2ZQR5xdvsrAqva3_7WcbbVbeJL4pj38HNVS2i9bL_pJfe6hKw9XVvRw2GpcmDOfWRNWAASuUhHD8apHPDrv7NMN29235gPMPQyzv3GSwFLZ0D24z2HGa4WGamZnl7CXpYoInapyOTZ7uo5fe3XP3nlRtFogAlMyJjmQgQpdTpdyE0ZDpTkf7vpBFkDLiIDQ_TKjnUqWT0JeuFJ4WRaEb7jpO4h2g1Qw2cYRwqBWMB5xQYPXA9nOmuBd1POXawn1KtNBFLcwY1NjGJnimzGIe1-JsocPyPOJpWW0jduF1BI7l8Z9zT9BGEespMgVPUVPDB6zO0JpY5ul8dl5oBzz7g6dv_s7I-g |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Identification+of+direct+transcriptional+target+genes+of+ExoS%2FChvI+two-component+signaling+in+Sinorhizobium+meliloti&rft.jtitle=Journal+of+bacteriology&rft.au=Chen%2C+Esther+J&rft.au=Fisher%2C+Robert+F&rft.au=Perovich%2C+Virginia+M&rft.au=Sabio%2C+Erich+A&rft.date=2009-11-01&rft.eissn=1098-5530&rft.volume=191&rft.issue=22&rft.spage=6833&rft.epage=6842&rft_id=info:doi/10.1128%2FJB.00734-09&rft.externalDBID=NO_FULL_TEXT |