Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan
Sinorhizobium meliloti enters into beneficial symbiotic interactions with Medicago species of legumes. Bacterial exopolysaccharides play critical signaling roles in infection thread initiation and growth during the early stages of root nodule formation. After endocytosis of S. meliloti by plant cell...
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American Society for Microbiology
2018
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| Online Access: | http://hdl.handle.net/1721.1/117433 https://orcid.org/0000-0002-1515-3582 https://orcid.org/0000-0002-3104-5856 https://orcid.org/0000-0001-7243-8261 |
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| author | Chen, Esther J. Penterman, Jon Shabab, Mohammed Arnold, Markus F. F. Walker, Graham C. |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Chen, Esther J. Penterman, Jon Shabab, Mohammed Arnold, Markus F. F. Walker, Graham C. |
| author_sort | Chen, Esther J. |
| collection | MIT |
| description | Sinorhizobium meliloti enters into beneficial symbiotic interactions with Medicago species of legumes. Bacterial exopolysaccharides play critical signaling roles in infection thread initiation and growth during the early stages of root nodule formation. After endocytosis of S. meliloti by plant cells in the developing nodule, plant-derived nodule-specific cysteine-rich (NCR) peptides mediate terminal differentiation of the bacteria into nitrogen-fixing bacteroids. Previous transcriptional studies showed that the intensively studied cationic peptide NCR247 induces expression of the exo genes that encode the proteins required for succinoglycan biosynthesis. In addition, genetic studies have shown that some exo mutants exhibit increased sensitivity to the antimicrobial action of NCR247. Therefore, we investigated whether the symbiotically active S. meliloti exopolysaccharide succinoglycan can protect S. meliloti against the antimicrobial activity of NCR247. We discovered that high-molecular-weight forms of succinoglycan have the ability to protect S. meliloti from the antimicrobial action of the NCR247 peptide but low-molecular-weight forms of wild-type succinoglycan do not. The protective function of high-molecular-weight succinoglycan occurs via direct molecular interactions between anionic succinoglycan and the cationic NCR247 peptide, but this interaction is not chiral. Taken together, our observations suggest that S. meliloti exopolysaccharides not only may be critical during early stages of nodule invasion but also are upregulated at a late stage of symbiosis to protect bacteria against the bactericidal action of cationic NCR peptides. Our findings represent an important step forward in fully understanding the complete set of exopolysaccharide functions during legume symbiosis. |
| first_indexed | 2024-09-23T14:58:25Z |
| format | Article |
| id | mit-1721.1/117433 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T14:58:25Z |
| publishDate | 2018 |
| publisher | American Society for Microbiology |
| record_format | dspace |
| spelling | mit-1721.1/1174332022-10-01T23:43:05Z Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan Chen, Esther J. Penterman, Jon Shabab, Mohammed Arnold, Markus F. F. Walker, Graham C. Massachusetts Institute of Technology. Department of Biology Walker, Graham Arnold, Markus Penterman, Jon Shabab, Mohammed Walker, Graham C Sinorhizobium meliloti enters into beneficial symbiotic interactions with Medicago species of legumes. Bacterial exopolysaccharides play critical signaling roles in infection thread initiation and growth during the early stages of root nodule formation. After endocytosis of S. meliloti by plant cells in the developing nodule, plant-derived nodule-specific cysteine-rich (NCR) peptides mediate terminal differentiation of the bacteria into nitrogen-fixing bacteroids. Previous transcriptional studies showed that the intensively studied cationic peptide NCR247 induces expression of the exo genes that encode the proteins required for succinoglycan biosynthesis. In addition, genetic studies have shown that some exo mutants exhibit increased sensitivity to the antimicrobial action of NCR247. Therefore, we investigated whether the symbiotically active S. meliloti exopolysaccharide succinoglycan can protect S. meliloti against the antimicrobial activity of NCR247. We discovered that high-molecular-weight forms of succinoglycan have the ability to protect S. meliloti from the antimicrobial action of the NCR247 peptide but low-molecular-weight forms of wild-type succinoglycan do not. The protective function of high-molecular-weight succinoglycan occurs via direct molecular interactions between anionic succinoglycan and the cationic NCR247 peptide, but this interaction is not chiral. Taken together, our observations suggest that S. meliloti exopolysaccharides not only may be critical during early stages of nodule invasion but also are upregulated at a late stage of symbiosis to protect bacteria against the bactericidal action of cationic NCR peptides. Our findings represent an important step forward in fully understanding the complete set of exopolysaccharide functions during legume symbiosis. 2018-08-20T20:07:16Z 2018-08-20T20:07:16Z 2018-06 2017-11 Article http://purl.org/eprint/type/JournalArticle 0021-9193 1098-5530 http://hdl.handle.net/1721.1/117433 Arnold, Markus F. F. et al. “Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan.” Edited by Yves V. Brun. Journal of Bacteriology 200, 13 (April 2018): e00665–17 © 2018 American Society for Microbiology https://orcid.org/0000-0002-1515-3582 https://orcid.org/0000-0002-3104-5856 https://orcid.org/0000-0001-7243-8261 en_US http://dx.doi.org/10.1128/JB.00665-17 Journal of Bacteriology Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf American Society for Microbiology Prof. Walker |
| spellingShingle | Chen, Esther J. Penterman, Jon Shabab, Mohammed Arnold, Markus F. F. Walker, Graham C. Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title | Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title_full | Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title_fullStr | Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title_full_unstemmed | Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title_short | Important Late-Stage Symbiotic Role of the Sinorhizobium Meliloti Exopolysaccharide Succinoglycan |
| title_sort | important late stage symbiotic role of the sinorhizobium meliloti exopolysaccharide succinoglycan |
| url | http://hdl.handle.net/1721.1/117433 https://orcid.org/0000-0002-1515-3582 https://orcid.org/0000-0002-3104-5856 https://orcid.org/0000-0001-7243-8261 |
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