Sinorhizobium fredii HH103 bacteroids are not terminally differentiated and show altered O-antigen in nodules of the Inverted Repeat-Lacking Clade legume Glycyrrhiza uralensis
Summary In rhizobial species that nodulate inverted repeat‐lacking clade (IRLC) legumes, such as the interaction between Sinorhizobium meliloti and Medicago, bacteroid differentiation is driven by an endoreduplication event that is induced by host nodule‐specific cysteine rich (NCR) antimicrobial pe...
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| Veröffentlicht in: | Environmental microbiology 2016-09, Vol.18 (8), p.2392-2404 |
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| creator | Crespo-Rivas, Juan C. Guefrachi, Ibtissem Mok, Kenny C. Villaécija-Aguilar, José A. Acosta-Jurado, Sebastián Pierre, Olivier Ruiz-Sainz, José E. Taga, Michiko E. Mergaert, Peter Vinardell, José M. |
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In rhizobial species that nodulate inverted repeat‐lacking clade (IRLC) legumes, such as the interaction between Sinorhizobium meliloti and Medicago, bacteroid differentiation is driven by an endoreduplication event that is induced by host nodule‐specific cysteine rich (NCR) antimicrobial peptides and requires the participation of the bacterial protein BacA. We have studied bacteroid differentiation of Sinorhizobium fredii HH103 in three host plants: Glycine max, Cajanus cajan and the IRLC legume Glycyrrhiza uralensis. Flow cytometry, microscopy analyses and viability studies of bacteroids as well as confocal microscopy studies carried out in nodules showed that S. fredii HH103 bacteroids, regardless of the host plant, had deoxyribonucleic acid (DNA) contents, cellular sizes and survival rates similar to those of free‐living bacteria. Contrary to S. meliloti, S. fredii HH103 showed little or no sensitivity to Medicago NCR247 and NCR335 peptides. Inactivation of S. fredii HH103 bacA neither affected symbiosis with Glycyrrhiza nor increased bacterial sensitivity to Medicago NCRs. Finally, HH103 bacteroids isolated from Glycyrrhiza, but not those isolated from Cajanus or Glycine, showed an altered lipopolysaccharide. Our studies indicate that, in contrast to the S. meliloti‐Medicago model symbiosis, bacteroids in the S. fredii HH103‐Glycyrrhiza symbiosis do not undergo NCR‐induced and bacA‐dependent terminal differentiation. |
| doi_str_mv | 10.1111/1462-2920.13101 |
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In rhizobial species that nodulate inverted repeat‐lacking clade (IRLC) legumes, such as the interaction between Sinorhizobium meliloti and Medicago, bacteroid differentiation is driven by an endoreduplication event that is induced by host nodule‐specific cysteine rich (NCR) antimicrobial peptides and requires the participation of the bacterial protein BacA. We have studied bacteroid differentiation of Sinorhizobium fredii HH103 in three host plants: Glycine max, Cajanus cajan and the IRLC legume Glycyrrhiza uralensis. Flow cytometry, microscopy analyses and viability studies of bacteroids as well as confocal microscopy studies carried out in nodules showed that S. fredii HH103 bacteroids, regardless of the host plant, had deoxyribonucleic acid (DNA) contents, cellular sizes and survival rates similar to those of free‐living bacteria. Contrary to S. meliloti, S. fredii HH103 showed little or no sensitivity to Medicago NCR247 and NCR335 peptides. Inactivation of S. fredii HH103 bacA neither affected symbiosis with Glycyrrhiza nor increased bacterial sensitivity to Medicago NCRs. Finally, HH103 bacteroids isolated from Glycyrrhiza, but not those isolated from Cajanus or Glycine, showed an altered lipopolysaccharide. Our studies indicate that, in contrast to the S. meliloti‐Medicago model symbiosis, bacteroids in the S. fredii HH103‐Glycyrrhiza symbiosis do not undergo NCR‐induced and bacA‐dependent terminal differentiation.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.13101</identifier><identifier>PMID: 26521863</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Bacterial Proteins - metabolism ; Glycyrrhiza uralensis - genetics ; Glycyrrhiza uralensis - microbiology ; Glycyrrhiza uralensis - physiology ; Inverted Repeat Sequences ; Life Sciences ; Lipopolysaccharides - metabolism ; O Antigens - genetics ; O Antigens - metabolism ; Root Nodules, Plant - genetics ; Root Nodules, Plant - microbiology ; Root Nodules, Plant - physiology ; Sinorhizobium fredii - genetics ; Sinorhizobium fredii - growth & development ; Sinorhizobium fredii - physiology ; Symbiosis</subject><ispartof>Environmental microbiology, 2016-09, Vol.18 (8), p.2392-2404</ispartof><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0009-0002-8050-8666 ; 0000-0002-5919-7317</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.13101$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.13101$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,777,781,882,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26521863$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01429983$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Crespo-Rivas, Juan C.</creatorcontrib><creatorcontrib>Guefrachi, Ibtissem</creatorcontrib><creatorcontrib>Mok, Kenny C.</creatorcontrib><creatorcontrib>Villaécija-Aguilar, José A.</creatorcontrib><creatorcontrib>Acosta-Jurado, Sebastián</creatorcontrib><creatorcontrib>Pierre, Olivier</creatorcontrib><creatorcontrib>Ruiz-Sainz, José E.</creatorcontrib><creatorcontrib>Taga, Michiko E.</creatorcontrib><creatorcontrib>Mergaert, Peter</creatorcontrib><creatorcontrib>Vinardell, José M.</creatorcontrib><title>Sinorhizobium fredii HH103 bacteroids are not terminally differentiated and show altered O-antigen in nodules of the Inverted Repeat-Lacking Clade legume Glycyrrhiza uralensis</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
In rhizobial species that nodulate inverted repeat‐lacking clade (IRLC) legumes, such as the interaction between Sinorhizobium meliloti and Medicago, bacteroid differentiation is driven by an endoreduplication event that is induced by host nodule‐specific cysteine rich (NCR) antimicrobial peptides and requires the participation of the bacterial protein BacA. We have studied bacteroid differentiation of Sinorhizobium fredii HH103 in three host plants: Glycine max, Cajanus cajan and the IRLC legume Glycyrrhiza uralensis. Flow cytometry, microscopy analyses and viability studies of bacteroids as well as confocal microscopy studies carried out in nodules showed that S. fredii HH103 bacteroids, regardless of the host plant, had deoxyribonucleic acid (DNA) contents, cellular sizes and survival rates similar to those of free‐living bacteria. Contrary to S. meliloti, S. fredii HH103 showed little or no sensitivity to Medicago NCR247 and NCR335 peptides. Inactivation of S. fredii HH103 bacA neither affected symbiosis with Glycyrrhiza nor increased bacterial sensitivity to Medicago NCRs. Finally, HH103 bacteroids isolated from Glycyrrhiza, but not those isolated from Cajanus or Glycine, showed an altered lipopolysaccharide. Our studies indicate that, in contrast to the S. meliloti‐Medicago model symbiosis, bacteroids in the S. fredii HH103‐Glycyrrhiza symbiosis do not undergo NCR‐induced and bacA‐dependent terminal differentiation.</description><subject>Bacterial Proteins - metabolism</subject><subject>Glycyrrhiza uralensis - genetics</subject><subject>Glycyrrhiza uralensis - microbiology</subject><subject>Glycyrrhiza uralensis - physiology</subject><subject>Inverted Repeat Sequences</subject><subject>Life Sciences</subject><subject>Lipopolysaccharides - metabolism</subject><subject>O Antigens - genetics</subject><subject>O Antigens - metabolism</subject><subject>Root Nodules, Plant - genetics</subject><subject>Root Nodules, Plant - microbiology</subject><subject>Root Nodules, Plant - physiology</subject><subject>Sinorhizobium fredii - genetics</subject><subject>Sinorhizobium fredii - growth & development</subject><subject>Sinorhizobium fredii - physiology</subject><subject>Symbiosis</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kctuEzEUhkcIREthzQ55CYsBX-ZiL6uoJJFCq1JuO8tjn0lMPZ7UnmkJKzY8EK_Ek-BpSrzxOf_5_mNLf5a9JPgtSecdKSqaU0FTywgmj7Ljg_L4UBN6lD2L8TvGpGY1fpod0aqkhFfsOPtzZX0fNvZn39ixQ20AY-3fX78XC4IZapQeIPTWRKQCIN8PKPWd9cq5HTK2bSGAH6wawCDlDYqb_g4pl6AkXOQqzdbgkfXJa0YHEfUtGjaAlv4WwuT6CFtQQ75S-tr6NZo5ZQA5WI8doLnb6V2YfqfQGJQDH218nj1plYvw4uE-yT6_P_s0W-Sri_lydrrKN7QoSF63qtFFoRVobQhPRVk1nDPBOddYQN1WghmBtVG0xYLWogQmdE0rxUVjGDvJ3uz3bpST22A7FXayV1YuTldy0jApqBCc3ZLEvt6z29DfjBAH2dmowTnloR-jJJzQ9HaNq4S-ekDHpgNz2Pw_kgSUe-DOOtgd5gTLKXE5ZSqnfOV94vLsw_K-SL5877NxgB8HnwrXskqxl_Lr-Vxe4m-X51-uuOTsHwnTr5A</recordid><startdate>20160901</startdate><enddate>20160901</enddate><creator>Crespo-Rivas, Juan C.</creator><creator>Guefrachi, Ibtissem</creator><creator>Mok, Kenny C.</creator><creator>Villaécija-Aguilar, José A.</creator><creator>Acosta-Jurado, Sebastián</creator><creator>Pierre, Olivier</creator><creator>Ruiz-Sainz, José E.</creator><creator>Taga, Michiko E.</creator><creator>Mergaert, Peter</creator><creator>Vinardell, José M.</creator><general>Blackwell Publishing Ltd</general><general>Society for Applied Microbiology and Wiley-Blackwell</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0009-0002-8050-8666</orcidid><orcidid>https://orcid.org/0000-0002-5919-7317</orcidid></search><sort><creationdate>20160901</creationdate><title>Sinorhizobium fredii HH103 bacteroids are not terminally differentiated and show altered O-antigen in nodules of the Inverted Repeat-Lacking Clade legume Glycyrrhiza uralensis</title><author>Crespo-Rivas, Juan C. ; Guefrachi, Ibtissem ; Mok, Kenny C. ; Villaécija-Aguilar, José A. ; Acosta-Jurado, Sebastián ; Pierre, Olivier ; Ruiz-Sainz, José E. ; Taga, Michiko E. ; Mergaert, Peter ; Vinardell, José M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-h2441-7fabc44caeccd184ca56b8839888c09e7f693d90cda2f092795e39c726a89bd33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Bacterial Proteins - metabolism</topic><topic>Glycyrrhiza uralensis - genetics</topic><topic>Glycyrrhiza uralensis - microbiology</topic><topic>Glycyrrhiza uralensis - physiology</topic><topic>Inverted Repeat Sequences</topic><topic>Life Sciences</topic><topic>Lipopolysaccharides - metabolism</topic><topic>O Antigens - genetics</topic><topic>O Antigens - metabolism</topic><topic>Root Nodules, Plant - genetics</topic><topic>Root Nodules, Plant - microbiology</topic><topic>Root Nodules, Plant - physiology</topic><topic>Sinorhizobium fredii - genetics</topic><topic>Sinorhizobium fredii - growth & development</topic><topic>Sinorhizobium fredii - physiology</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Crespo-Rivas, Juan C.</creatorcontrib><creatorcontrib>Guefrachi, Ibtissem</creatorcontrib><creatorcontrib>Mok, Kenny C.</creatorcontrib><creatorcontrib>Villaécija-Aguilar, José A.</creatorcontrib><creatorcontrib>Acosta-Jurado, Sebastián</creatorcontrib><creatorcontrib>Pierre, Olivier</creatorcontrib><creatorcontrib>Ruiz-Sainz, José E.</creatorcontrib><creatorcontrib>Taga, Michiko E.</creatorcontrib><creatorcontrib>Mergaert, Peter</creatorcontrib><creatorcontrib>Vinardell, José M.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Crespo-Rivas, Juan C.</au><au>Guefrachi, Ibtissem</au><au>Mok, Kenny C.</au><au>Villaécija-Aguilar, José A.</au><au>Acosta-Jurado, Sebastián</au><au>Pierre, Olivier</au><au>Ruiz-Sainz, José E.</au><au>Taga, Michiko E.</au><au>Mergaert, Peter</au><au>Vinardell, José M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sinorhizobium fredii HH103 bacteroids are not terminally differentiated and show altered O-antigen in nodules of the Inverted Repeat-Lacking Clade legume Glycyrrhiza uralensis</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2016-09-01</date><risdate>2016</risdate><volume>18</volume><issue>8</issue><spage>2392</spage><epage>2404</epage><pages>2392-2404</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
In rhizobial species that nodulate inverted repeat‐lacking clade (IRLC) legumes, such as the interaction between Sinorhizobium meliloti and Medicago, bacteroid differentiation is driven by an endoreduplication event that is induced by host nodule‐specific cysteine rich (NCR) antimicrobial peptides and requires the participation of the bacterial protein BacA. We have studied bacteroid differentiation of Sinorhizobium fredii HH103 in three host plants: Glycine max, Cajanus cajan and the IRLC legume Glycyrrhiza uralensis. Flow cytometry, microscopy analyses and viability studies of bacteroids as well as confocal microscopy studies carried out in nodules showed that S. fredii HH103 bacteroids, regardless of the host plant, had deoxyribonucleic acid (DNA) contents, cellular sizes and survival rates similar to those of free‐living bacteria. Contrary to S. meliloti, S. fredii HH103 showed little or no sensitivity to Medicago NCR247 and NCR335 peptides. Inactivation of S. fredii HH103 bacA neither affected symbiosis with Glycyrrhiza nor increased bacterial sensitivity to Medicago NCRs. Finally, HH103 bacteroids isolated from Glycyrrhiza, but not those isolated from Cajanus or Glycine, showed an altered lipopolysaccharide. Our studies indicate that, in contrast to the S. meliloti‐Medicago model symbiosis, bacteroids in the S. fredii HH103‐Glycyrrhiza symbiosis do not undergo NCR‐induced and bacA‐dependent terminal differentiation.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26521863</pmid><doi>10.1111/1462-2920.13101</doi><tpages>13</tpages><orcidid>https://orcid.org/0009-0002-8050-8666</orcidid><orcidid>https://orcid.org/0000-0002-5919-7317</orcidid></addata></record> |
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| subjects | Bacterial Proteins - metabolism Glycyrrhiza uralensis - genetics Glycyrrhiza uralensis - microbiology Glycyrrhiza uralensis - physiology Inverted Repeat Sequences Life Sciences Lipopolysaccharides - metabolism O Antigens - genetics O Antigens - metabolism Root Nodules, Plant - genetics Root Nodules, Plant - microbiology Root Nodules, Plant - physiology Sinorhizobium fredii - genetics Sinorhizobium fredii - growth & development Sinorhizobium fredii - physiology Symbiosis |
| title | Sinorhizobium fredii HH103 bacteroids are not terminally differentiated and show altered O-antigen in nodules of the Inverted Repeat-Lacking Clade legume Glycyrrhiza uralensis |
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