Mannose metabolism is required for mycobacterial growth
Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant cell-wall mannolipids (phosphatidylinositol mannosides, lipoarabinomannan), a cytoplasmic methylmannose polysaccharide and O-mannosylated glycoprote...
Saved in:
| Published in: | Biochemical journal Vol. 372; no. Pt 1; p. 77 |
|---|---|
| Main Authors: | , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
England
15.05.2003
|
| Subjects: | |
| ISSN: | 0264-6021 |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant cell-wall mannolipids (phosphatidylinositol mannosides, lipoarabinomannan), a cytoplasmic methylmannose polysaccharide and O-mannosylated glycoproteins. To investigate whether these molecules are essential for mycobacterial growth, we have generated a Mycobacterium smegmatis mannose auxotroph by targeted deletion of the gene encoding phosphomannose isomerase (PMI). The PMI deletion mutant displayed a mild hyperseptation phenotype, but grew normally in media containing an exogenous source of mannose. When this mutant was suspended in media without mannose, ongoing synthesis of both the mannolipids and methylmannose polysaccharides was halted and the hyperseptation phenotype became more pronounced. These changes preceded a dramatic loss of viability after 10 h in mannose-free media. Mannose starvation did not lead to detectable changes in cell-wall ultrastructure or permeability to hydrophobic drugs, or to changes in the rate of biosynthesis of other plasma-membrane or wall-associated phospholipids. These results show that mannose metabolism is required for growth of M. smegmatis and that one or more mannose-containing molecules may play a role in regulating septation and cell division in these bacteria. |
|---|---|
| AbstractList | Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant cell-wall mannolipids (phosphatidylinositol mannosides, lipoarabinomannan), a cytoplasmic methylmannose polysaccharide and O-mannosylated glycoproteins. To investigate whether these molecules are essential for mycobacterial growth, we have generated a Mycobacterium smegmatis mannose auxotroph by targeted deletion of the gene encoding phosphomannose isomerase (PMI). The PMI deletion mutant displayed a mild hyperseptation phenotype, but grew normally in media containing an exogenous source of mannose. When this mutant was suspended in media without mannose, ongoing synthesis of both the mannolipids and methylmannose polysaccharides was halted and the hyperseptation phenotype became more pronounced. These changes preceded a dramatic loss of viability after 10 h in mannose-free media. Mannose starvation did not lead to detectable changes in cell-wall ultrastructure or permeability to hydrophobic drugs, or to changes in the rate of biosynthesis of other plasma-membrane or wall-associated phospholipids. These results show that mannose metabolism is required for growth of M. smegmatis and that one or more mannose-containing molecules may play a role in regulating septation and cell division in these bacteria. Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant cell-wall mannolipids (phosphatidylinositol mannosides, lipoarabinomannan), a cytoplasmic methylmannose polysaccharide and O-mannosylated glycoproteins. To investigate whether these molecules are essential for mycobacterial growth, we have generated a Mycobacterium smegmatis mannose auxotroph by targeted deletion of the gene encoding phosphomannose isomerase (PMI). The PMI deletion mutant displayed a mild hyperseptation phenotype, but grew normally in media containing an exogenous source of mannose. When this mutant was suspended in media without mannose, ongoing synthesis of both the mannolipids and methylmannose polysaccharides was halted and the hyperseptation phenotype became more pronounced. These changes preceded a dramatic loss of viability after 10 h in mannose-free media. Mannose starvation did not lead to detectable changes in cell-wall ultrastructure or permeability to hydrophobic drugs, or to changes in the rate of biosynthesis of other plasma-membrane or wall-associated phospholipids. These results show that mannose metabolism is required for growth of M. smegmatis and that one or more mannose-containing molecules may play a role in regulating septation and cell division in these bacteria.Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant cell-wall mannolipids (phosphatidylinositol mannosides, lipoarabinomannan), a cytoplasmic methylmannose polysaccharide and O-mannosylated glycoproteins. To investigate whether these molecules are essential for mycobacterial growth, we have generated a Mycobacterium smegmatis mannose auxotroph by targeted deletion of the gene encoding phosphomannose isomerase (PMI). The PMI deletion mutant displayed a mild hyperseptation phenotype, but grew normally in media containing an exogenous source of mannose. When this mutant was suspended in media without mannose, ongoing synthesis of both the mannolipids and methylmannose polysaccharides was halted and the hyperseptation phenotype became more pronounced. These changes preceded a dramatic loss of viability after 10 h in mannose-free media. Mannose starvation did not lead to detectable changes in cell-wall ultrastructure or permeability to hydrophobic drugs, or to changes in the rate of biosynthesis of other plasma-membrane or wall-associated phospholipids. These results show that mannose metabolism is required for growth of M. smegmatis and that one or more mannose-containing molecules may play a role in regulating septation and cell division in these bacteria. |
| Author | Jeevarajah, Dharshini Waller, Ross F Billman-Jacobe, Helen Patterson, John H McConville, Malcolm J |
| Author_xml | – sequence: 1 givenname: John H surname: Patterson fullname: Patterson, John H organization: Department of Biochemistry and Molecular Biology, University of Melbourne, Parkville, Victoria 3010, Australia – sequence: 2 givenname: Ross F surname: Waller fullname: Waller, Ross F – sequence: 3 givenname: Dharshini surname: Jeevarajah fullname: Jeevarajah, Dharshini – sequence: 4 givenname: Helen surname: Billman-Jacobe fullname: Billman-Jacobe, Helen – sequence: 5 givenname: Malcolm J surname: McConville fullname: McConville, Malcolm J |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/12593673$$D View this record in MEDLINE/PubMed |
| BookMark | eNo1j0tLw0AURmdRsQ_d-AMkK3fRO3ceaZZSfEHFja7DzeSOpiSZdiZB-u8VrKvDB4cPzlLMhjCwEFcSbiVovKt3CICyAJiJBaDVuf2dc7FMaQcgNWg4F3OJplS2UAtRvNIwhMRZzyPVoWtTn7Upi3yY2shN5kPM-qMLNbmRY0td9hnD9_h1Ic48dYkvT1yJj8eH981zvn17etncb3OnwYy5B2md0tZw2VhLklAVUhuDpJ03Zu1oTegsunVTl6UFJxV5KhU0JXr2Ba7Ezd_vPobDxGms-jY57joaOEypKhQaA9b8itcncap7bqp9bHuKx-o_FX8AxoJUOA |
| CitedBy_id | crossref_primary_10_1016_j_bmc_2009_09_005 crossref_primary_10_1016_j_mam_2016_04_004 crossref_primary_10_1016_j_jmgm_2006_01_001 crossref_primary_10_1074_jbc_M110_165407 crossref_primary_10_1016_j_micpath_2016_10_008 crossref_primary_10_3390_app10072278 crossref_primary_10_1016_j_bmcl_2004_04_103 crossref_primary_10_1186_0717_6287_47_42 crossref_primary_10_1186_gb_2007_8_5_r89 crossref_primary_10_1016_j_tube_2008_01_003 crossref_primary_10_1038_s41467_024_46565_5 crossref_primary_10_1074_jbc_M604214200 crossref_primary_10_1021_jacs_3c09495 crossref_primary_10_1017_S0031182016002377 crossref_primary_10_1074_jbc_R110_168328 crossref_primary_10_1371_journal_pone_0028476 crossref_primary_10_1016_j_biochi_2010_07_016 crossref_primary_10_1107_S2059798319004169 crossref_primary_10_1074_jbc_M414181200 crossref_primary_10_1371_journal_pone_0108854 crossref_primary_10_1042_BCJ20200194 crossref_primary_10_1007_s00253_010_3002_8 crossref_primary_10_1039_c000604a crossref_primary_10_1021_bi035688h crossref_primary_10_3109_10409238_2014_925420 crossref_primary_10_1016_j_tube_2010_02_003 crossref_primary_10_1016_j_ymben_2008_08_007 crossref_primary_10_1002_jcc_24503 crossref_primary_10_1128_IAI_05635_11 crossref_primary_10_1128_microbiolspec_MGM2_0013_2013 crossref_primary_10_1002_jcc_20586 crossref_primary_10_1016_j_tim_2004_03_002 |
| ContentType | Journal Article |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1042/bj20021700 |
| 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 MEDLINE - Academic |
| 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 | Anatomy & Physiology Chemistry |
| ExternalDocumentID | 12593673 |
| Genre | Research Support, Non-U.S. Gov't Journal Article |
| GroupedDBID | --- -DZ -~X .55 .GJ 0R~ 23N 2WC 3EH 3O- 4.4 53G 5GY 5RE 5VS 6J9 79B AABGO AAHRG ABJNI ABPPZ ABTAH ACGFO ACGFS ACNCT ADBBV AEGXH AENEX AI. AIAGR AIZAD ALMA_UNASSIGNED_HOLDINGS BAWUL CGR CS3 CUY CVF DU5 E3Z EBS ECM EIF EJD F5P H13 HH6 HYE HZ~ K-O L7B MV1 MVM N9A NPM O9- OHT OK1 P2P RHI RNS RPM RPO TR2 TWZ VH1 VXZ WH7 WOQ X7M XOL XSW Y6R YNY ZGI ZXP ZY4 ~02 ~KM 7X8 ADXHL |
| ID | FETCH-LOGICAL-c405t-f016c3465e9d66a1a23714552a4cf558ca8a2c62c8db9960c13afa930d92fef72 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 56 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000183070800007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 0264-6021 |
| IngestDate | Fri Jul 11 11:17:31 EDT 2025 Wed Feb 19 01:38:32 EST 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | Pt 1 |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c405t-f016c3465e9d66a1a23714552a4cf558ca8a2c62c8db9960c13afa930d92fef72 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | https://portlandpress.com/biochemj/article-pdf/372/1/77/711307/bj3720077.pdf |
| PMID | 12593673 |
| PQID | 73255065 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_73255065 pubmed_primary_12593673 |
| PublicationCentury | 2000 |
| PublicationDate | 2003-May-15 20030515 |
| PublicationDateYYYYMMDD | 2003-05-15 |
| PublicationDate_xml | – month: 05 year: 2003 text: 2003-May-15 day: 15 |
| PublicationDecade | 2000 |
| PublicationPlace | England |
| PublicationPlace_xml | – name: England |
| PublicationTitle | Biochemical journal |
| PublicationTitleAlternate | Biochem J |
| PublicationYear | 2003 |
| References | 11257028 - Antimicrob Agents Chemother. 2001 Apr;45(4):1143-50 1904554 - Nature. 1991 Jun 6;351(6326):456-60 885878 - J Biol Chem. 1977 Aug 25;252(16):5735-9 7364726 - J Bacteriol. 1980 Mar;141(3):1217-21 7759478 - J Biol Chem. 1995 May 26;270(21):12380-9 11677227 - J Biol Chem. 2001 Dec 28;276(52):48854-62 6237955 - Gene. 1984 Sep;29(3):303-13 11931640 - Biochem J. 2002 Jul 15;365(Pt 2):441-50 7574484 - Annu Rev Biochem. 1995;64:29-63 10959727 - Int J Med Microbiol. 2000 Jul;290(3):251-8 11084042 - J Biol Chem. 2001 Mar 2;276(9):6566-75 885879 - J Biol Chem. 1977 Aug 25;252(16):5740-4 6706967 - J Biol Chem. 1984 Mar 25;259(6):3464-9 7772860 - Glycobiology. 1995 Feb;5(1):117-27 9529150 - Immunity. 1998 Mar;8(3):331-40 8489004 - Anal Biochem. 1993 Apr;210(1):106-12 4887011 - J Ultrastruct Res. 1969 Jan;26(1):31-43 2082148 - Mol Microbiol. 1990 Nov;4(11):1911-9 8626314 - J Bacteriol. 1996 May;178(9):2498-506 856790 - J Biol Chem. 1977 Apr 25;252(8):2459-69 12122024 - Glycobiology. 2002 Jul;12(7):427-34 9925791 - J Mol Biol. 1999 Feb 5;285(5):2147-60 11964144 - Biochem J. 2002 May 1;363(Pt 3):437-47 457682 - J Biol Chem. 1979 Aug 10;254(15):7282-6 8955410 - J Bacteriol. 1996 Dec;178(24):7254-9 6841516 - J Chromatogr. 1983 Feb 18;256(3):419-27 9634230 - Nature. 1998 Jun 11;393(6685):537-44 10531370 - J Biol Chem. 1999 Oct 29;274(44):31625-31 10510238 - Mol Microbiol. 1999 Sep;33(6):1244-53 9401044 - J Bacteriol. 1997 Dec;179(24):7827-33 12147678 - J Cell Biol. 2002 Aug 5;158(3):421-6 12068013 - J Biol Chem. 2002 Aug 30;277(35):31335-44 10656114 - Tuber Lung Dis. 1999;79(3):153-69 7622204 - Infect Immun. 1995 Aug;63(8):2846-53 9705430 - J Clin Microbiol. 1998 Sep;36(9):2752-4 10889206 - J Biol Chem. 2000 Sep 29;275(39):30092-9 9451020 - Glycobiology. 1998 Feb;8(2):113-20 |
| References_xml | – reference: 8626314 - J Bacteriol. 1996 May;178(9):2498-506 – reference: 7364726 - J Bacteriol. 1980 Mar;141(3):1217-21 – reference: 7772860 - Glycobiology. 1995 Feb;5(1):117-27 – reference: 7622204 - Infect Immun. 1995 Aug;63(8):2846-53 – reference: 6237955 - Gene. 1984 Sep;29(3):303-13 – reference: 10531370 - J Biol Chem. 1999 Oct 29;274(44):31625-31 – reference: 7574484 - Annu Rev Biochem. 1995;64:29-63 – reference: 10510238 - Mol Microbiol. 1999 Sep;33(6):1244-53 – reference: 9401044 - J Bacteriol. 1997 Dec;179(24):7827-33 – reference: 856790 - J Biol Chem. 1977 Apr 25;252(8):2459-69 – reference: 1904554 - Nature. 1991 Jun 6;351(6326):456-60 – reference: 8489004 - Anal Biochem. 1993 Apr;210(1):106-12 – reference: 9705430 - J Clin Microbiol. 1998 Sep;36(9):2752-4 – reference: 9925791 - J Mol Biol. 1999 Feb 5;285(5):2147-60 – reference: 12122024 - Glycobiology. 2002 Jul;12(7):427-34 – reference: 10889206 - J Biol Chem. 2000 Sep 29;275(39):30092-9 – reference: 10959727 - Int J Med Microbiol. 2000 Jul;290(3):251-8 – reference: 9634230 - Nature. 1998 Jun 11;393(6685):537-44 – reference: 6706967 - J Biol Chem. 1984 Mar 25;259(6):3464-9 – reference: 11677227 - J Biol Chem. 2001 Dec 28;276(52):48854-62 – reference: 10656114 - Tuber Lung Dis. 1999;79(3):153-69 – reference: 11964144 - Biochem J. 2002 May 1;363(Pt 3):437-47 – reference: 6841516 - J Chromatogr. 1983 Feb 18;256(3):419-27 – reference: 11257028 - Antimicrob Agents Chemother. 2001 Apr;45(4):1143-50 – reference: 11931640 - Biochem J. 2002 Jul 15;365(Pt 2):441-50 – reference: 12068013 - J Biol Chem. 2002 Aug 30;277(35):31335-44 – reference: 885879 - J Biol Chem. 1977 Aug 25;252(16):5740-4 – reference: 457682 - J Biol Chem. 1979 Aug 10;254(15):7282-6 – reference: 4887011 - J Ultrastruct Res. 1969 Jan;26(1):31-43 – reference: 7759478 - J Biol Chem. 1995 May 26;270(21):12380-9 – reference: 8955410 - J Bacteriol. 1996 Dec;178(24):7254-9 – reference: 885878 - J Biol Chem. 1977 Aug 25;252(16):5735-9 – reference: 9529150 - Immunity. 1998 Mar;8(3):331-40 – reference: 11084042 - J Biol Chem. 2001 Mar 2;276(9):6566-75 – reference: 2082148 - Mol Microbiol. 1990 Nov;4(11):1911-9 – reference: 12147678 - J Cell Biol. 2002 Aug 5;158(3):421-6 – reference: 9451020 - Glycobiology. 1998 Feb;8(2):113-20 |
| SSID | ssj0014040 |
| Score | 1.9817183 |
| Snippet | Mycobacteria are the causative agents of tuberculosis and several other significant diseases in humans. All species of mycobacteria synthesize abundant... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | 77 |
| SubjectTerms | beta-Mannosidase Cell Division - physiology Fatty Acids - biosynthesis Mannose - metabolism Mannose-6-Phosphate Isomerase - genetics Mannose-6-Phosphate Isomerase - metabolism Mannosidases - genetics Mannosidases - metabolism Microscopy, Electron Molecular Sequence Data Mycobacterium smegmatis - genetics Mycobacterium smegmatis - growth & development Mycobacterium smegmatis - metabolism Mycobacterium smegmatis - ultrastructure |
| Title | Mannose metabolism is required for mycobacterial growth |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/12593673 https://www.proquest.com/docview/73255065 |
| Volume | 372 |
| WOSCitedRecordID | wos000183070800007&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/eLvHCXMwpV3JTsMwEB0VigQXlpalrD4gbhFpYsexhIRKRYUQVD0A6q1yvUAlkpamIPXvGbuNOCEOXKLkkM3xeJ7HL-8BnAvFDdW6GZjIOguzIXMxZ3GPDSXOD4Tx1gkvD7zbTft90avAVfkvjKNVlmOiH6j1WLka-SWPEfxivryefATOM8qtrS4NNFagGiOQcYQu3v9ZQ6AhXVZYaJBgKivFSWl0eXPvuQk8DH8Hlj7BdLb-92jbsLkElqS16Ak7UDF5DeqtHCfV2ZxcEE_19DX0Gqy3S5u3OnBnkzwuDMnMDDvE-6jIyKggU-MowkYTBLUkmysMey_rjLd4xZn77G0Xnju3T-27YOmmECgEZbPAIrhTMU2YETpJZFNGTqyPsUhSZRlLlUxlpJJIpXroJFtUM5ZWijjUIrLG8mgPVvNxbg6ApMKEWoqhZVTih3ZEfjzm1OomXluqBpyVDTXAt3FLEDI3489iUDZVA_YXbT2YLEQ1Bgi0RJzw-PDPc49gwzPqnIQqO4aqxTg1J7CmvmajYnrqOwFuu73Hb8bXvRw |
| 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=Mannose+metabolism+is+required+for+mycobacterial+growth&rft.jtitle=Biochemical+journal&rft.au=Patterson%2C+John+H&rft.au=Waller%2C+Ross+F&rft.au=Jeevarajah%2C+Dharshini&rft.au=Billman-Jacobe%2C+Helen&rft.date=2003-05-15&rft.issn=0264-6021&rft.volume=372&rft.issue=Pt+1&rft.spage=77&rft_id=info:doi/10.1042%2Fbj20021700&rft_id=info%3Apmid%2F12593673&rft_id=info%3Apmid%2F12593673&rft.externalDocID=12593673 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0264-6021&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0264-6021&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0264-6021&client=summon |