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Title: Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight

Abstract

ABSTRACT The acidic polysaccharide succinoglycan produced by the rhizobial symbiontSinorhizobium meliloti1021 is required for this bacterium to invade the host plantMedicago truncatulaand establish a nitrogen-fixing symbiosis.S. melilotimutants that cannot make succinoglycan cannot initiate invasion structures called infection threads in plant root hairs.S. melilotiexoH mutants that cannot succinylate succinoglycan are also unable to form infection threads, despite the fact that they make large quantities of succinoglycan. Succinoglycan produced byexoHmutants is refractory to cleavage by the glycanases encoded byexoKandexsH, and thus succinoglycan produced byexoHmutants is made only in the high-molecular-weight (HMW) form. One interpretation of the symbiotic defect ofexoHmutants is that the low-molecular-weight (LMW) form of succinoglycan is required for infection thread formation. However, our data demonstrate that production of the HMW form of succinoglycan byS. meliloti1021 is sufficient for invasion of the hostM. truncatulaand that the LMW form is not required. Here, we show thatS. melilotistrains deficient in theexoK- andexsH-encoded glycanases invadeM. truncatulaand form a productive symbiosis, although they do this with somewhat less efficiency than the wild type. We have also characterized the polysaccharides produced by these double glycanase mutants and determined that they consist of only HMW succinoglycan and no detectable LMW succinoglycan. This demonstrates that LMW succinoglycan is not required for host invasion. Thesemore » results suggest succinoglycan function is not dependent upon the presence of a small, readily diffusible form. IMPORTANCESinorhizobium melilotiis a bacterium that forms a beneficial symbiosis with legume host plants.S. melilotiand other rhizobia convert atmospheric nitrogen to ammonia, a nutrient source for the host plant. To establish the symbiosis, rhizobia must invade plant roots, supplying the proper signals to prevent a plant immune response during invasion. A polysaccharide, succinoglycan, produced byS. melilotiis required for successful invasion. Here, we show that the critical feature of succinoglycan that allows infection to proceed is the attachment of a “succinyl” chemical group and that the chain length of succinoglycan is much less important for its function. We also show that none of the short-chain versions of succinoglycan is produced in the absence of two chain-cleaving enzymes.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Florida State Univ., Tallahassee, FL (United States). Dept. of Biological Science
Publication Date:
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1626114
Grant/Contract Number:  
FG02-93ER20097; USDA-NIFA [2014-67013-21579]
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Volume: 7; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology

Citation Formats

Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, and Jones, Kathryn M. Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight. United States: N. p., 2016. Web. doi:10.1128/mbio.00606-16.
Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, & Jones, Kathryn M. Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight. United States. doi:10.1128/mbio.00606-16.
Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, and Jones, Kathryn M. Tue . "Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight". United States. doi:10.1128/mbio.00606-16. https://www.osti.gov/servlets/purl/1626114.
@article{osti_1626114,
title = {Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight},
author = {Mendis, Hajeewaka C. and Madzima, Thelma F. and Queiroux, Clothilde and Jones, Kathryn M.},
abstractNote = {ABSTRACT The acidic polysaccharide succinoglycan produced by the rhizobial symbiontSinorhizobium meliloti1021 is required for this bacterium to invade the host plantMedicago truncatulaand establish a nitrogen-fixing symbiosis.S. melilotimutants that cannot make succinoglycan cannot initiate invasion structures called infection threads in plant root hairs.S. melilotiexoH mutants that cannot succinylate succinoglycan are also unable to form infection threads, despite the fact that they make large quantities of succinoglycan. Succinoglycan produced byexoHmutants is refractory to cleavage by the glycanases encoded byexoKandexsH, and thus succinoglycan produced byexoHmutants is made only in the high-molecular-weight (HMW) form. One interpretation of the symbiotic defect ofexoHmutants is that the low-molecular-weight (LMW) form of succinoglycan is required for infection thread formation. However, our data demonstrate that production of the HMW form of succinoglycan byS. meliloti1021 is sufficient for invasion of the hostM. truncatulaand that the LMW form is not required. Here, we show thatS. melilotistrains deficient in theexoK- andexsH-encoded glycanases invadeM. truncatulaand form a productive symbiosis, although they do this with somewhat less efficiency than the wild type. We have also characterized the polysaccharides produced by these double glycanase mutants and determined that they consist of only HMW succinoglycan and no detectable LMW succinoglycan. This demonstrates that LMW succinoglycan is not required for host invasion. These results suggest succinoglycan function is not dependent upon the presence of a small, readily diffusible form. IMPORTANCESinorhizobium melilotiis a bacterium that forms a beneficial symbiosis with legume host plants.S. melilotiand other rhizobia convert atmospheric nitrogen to ammonia, a nutrient source for the host plant. To establish the symbiosis, rhizobia must invade plant roots, supplying the proper signals to prevent a plant immune response during invasion. A polysaccharide, succinoglycan, produced byS. melilotiis required for successful invasion. Here, we show that the critical feature of succinoglycan that allows infection to proceed is the attachment of a “succinyl” chemical group and that the chain length of succinoglycan is much less important for its function. We also show that none of the short-chain versions of succinoglycan is produced in the absence of two chain-cleaving enzymes.},
doi = {10.1128/mbio.00606-16},
journal = {mBio (Online)},
issn = {2150-7511},
number = 3,
volume = 7,
place = {United States},
year = {2016},
month = {6}
}

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