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Extended hopanoid loss reduces bacterial motility and surface attachment, and leads to heterogeneity in root nodule growth kinetics in a Bradyrhizobium-Aeschynomene symbiosis

Belin, Brittany J. and Tookmanian, Elise T. and de Anda, Jaime and Wong, Gerard C. L. and Newman, Dianne (2019) Extended hopanoid loss reduces bacterial motility and surface attachment, and leads to heterogeneity in root nodule growth kinetics in a Bradyrhizobium-Aeschynomene symbiosis. Molecular Plant-Microbe Interactions, 32 (10). pp. 1415-1428. ISSN 0894-0282.

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Hopanoids are steroid-like bacterial lipids that enhance membrane rigidity and promote bacterial growth under diverse stresses. Roughly 10% of bacteria contain genes involved in hopanoid biosynthesis, and these genes are particularly conserved in plant-associated organisms. We previously found that the extended class of hopanoids (C35) in the nitrogen-fixing soil bacterium Bradyrhizobium diazoefficiens promotes its root nodule symbiosis with the tropical legume Aeschynomene afraspera. By quantitatively modeling root nodule development, we identify independent consequences of extended hopanoid loss in the initiation of root nodule formation and in the rate of root nodule maturation. In vitro studies demonstrate that extended hopanoids support B. diazoefficiens motility and surface attachment, which may correlate with stable root colonization in planta. Confocal microscopy of maturing root nodules reveals that root nodules infected with extended hopanoid-deficient B. diazoefficiens contain unusually low densities of bacterial symbionts, indicating that extended hopanoids are necessary for persistent, high levels of host infection.

Item Type:Article
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URLURL TypeDescription Paper
de Anda, Jaime0000-0003-2129-0775
Wong, Gerard C. L.0000-0003-0893-6383
Newman, Dianne0000-0003-1647-1918
Additional Information:© 2019 The American Phytopathological Society. This work was supported by grants from the HHMI (D.K.N.), NASA (NNX12AD93G, D.K.N.), Jane Coffin Childs Memorial Fund (B.J.B.), NIH (K99GM126141, B.J.B.), and Army Research Office (W911NF-18-1-0254, GW) and predoctoral 635 fellowships from NSF (E.T.) and the Ford Foundation (J.d.A.). We thank Dr. Eric Giraud for his generous gift of A. afraspera seeds and training on Aeschynomene symbioses and Drs. Hans-Martin Fischer and Raphael Ledermann for plasmids and technical advice for the genetic transformation of B. diazoefficiens. Dr. Nathan Dalleska of the Environmental Analysis Center at Caltech was instrumental in providing training and support for GC-MS analysis of acetylene reduction. We are grateful to Dr. Gargi Kulkarni and other members of the Newman lab, as well as Drs. Elliot Meyerowitz and Rob Phillips, for their collegiality and thoughtful discussions about this work. We are indebted to Ms. Shannon Park and Ms. Kristy Nguyen for providing the administrative assistance that allows us to focus on our research.
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Jane Coffin Childs Memorial Fund for Medical ResearchUNSPECIFIED
Army Research Office (ARO)W911NF-18-1-0254
Ford FoundationUNSPECIFIED
Issue or Number:10
Record Number:CaltechAUTHORS:20181218-110603835
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Official Citation:Extended Hopanoid Loss Reduces Bacterial Motility and Surface Attachment and Leads to Heterogeneity in Root Nodule Growth Kinetics in a Bradyrhizobium-Aeschynomene Symbiosis Brittany J. Belin, Elise M. Tookmanian, Jaime de Anda, Gerard C. L. Wong, and Dianne K. Newman Molecular Plant-Microbe Interactions 2019 32:10, 1415-1428.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:91894
Deposited By: Tony Diaz
Deposited On:18 Dec 2018 19:14
Last Modified:07 Apr 2020 16:15

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