Root-secreted Nucleosides: Signaling Chemoattractants of Rhizosphere Bacteria

Overview

Journal Front Plant Sci

Date 2024 May 27

PMID 38799096

Authors

Guy Keren

Galit Yehezkel

Lakkakula Satish

Zahar Adamov

Zeev Barak

Shimon Ben-Shabat

Varda Kagan-Zur

Yaron Sitrit

Affiliations

Soon will be listed here.

Abstract

The rhizosphere is a complex ecosystem, consisting of a narrow soil zone influenced by plant roots and inhabited by soil-borne microorganisms. Plants actively shape the rhizosphere microbiome through root exudates. Some metabolites are signaling molecules specifically functioning as chemoattractants rather than nutrients. These elusive signaling molecules have been sought for several decades, and yet little progress has been made. Root-secreted nucleosides and deoxynucleosides were detected in exudates of various plants by targeted ultra-performance liquid chromatography-mass spectrometry/mass spectrometry. Rhizobacteria were isolated from the roots of carrying the mycorrhizal desert truffle . Chemotaxis was determined by a glass capillary assay or plate assays on semisolid agar and through a soil plate assay. Nucleosides were identified in root exudates of plants that inhabit diverse ecological niches. Nucleosides induced positive chemotaxis in plant beneficial bacteria , , spp., , and the pathogenic rhizobacterium and . In a soil plate assay, nucleosides diffused to substantial distances and evoked chemotaxis under conditions as close as possible to natural environments. This study implies that root-secreted nucleosides are involved in the assembly of the rhizosphere bacterial community by inducing chemotaxis toward plant roots. In animals, nucleoside secretion known as "purinergic signaling" is involved in communication between cells, physiological processes, diseases, phagocytic cell migration, and bacterial activity. The coliform bacterium that inhabits the lower intestine of warm-blooded organisms also attracted to nucleosides, implying that nucleosides may serve as a common signal for bacterial species inhabiting distinct habitats. Taken together, all these may indicate that chemotaxis signaling by nucleosides is a conserved universal mechanism that encompasses living kingdoms and environments and should be given further attention in plant rhizosphere microbiome research.

References

Massalha H, Korenblum E, Malitsky S, Shapiro O, Aharoni A . Live imaging of root-bacteria interactions in a microfluidics setup. Proc Natl Acad Sci U S A. 2017; 114(17):4549-4554. PMC: 5410799. DOI: 10.1073/pnas.1618584114. View

Strehmel N, Bottcher C, Schmidt S, Scheel D . Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry. 2014; 108:35-46. DOI: 10.1016/j.phytochem.2014.10.003. View

Raina J, Fernandez V, Lambert B, Stocker R, Seymour J . The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol. 2019; 17(5):284-294. DOI: 10.1038/s41579-019-0182-9. View

Feng H, Fu R, Hou X, Lv Y, Zhang N, Liu Y . Chemotaxis of Beneficial Rhizobacteria to Root Exudates: The First Step towards Root-Microbe Rhizosphere Interactions. Int J Mol Sci. 2021; 22(13). PMC: 8269324. DOI: 10.3390/ijms22136655. View

Wadhams G, Armitage J . Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol. 2004; 5(12):1024-37. DOI: 10.1038/nrm1524. View

Ryan R, Vorholter F, Potnis N, Jones J, Van Sluys M, Bogdanove A . Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol. 2011; 9(5):344-55. DOI: 10.1038/nrmicro2558. View

Saxild H, Andersen L, Hammer K . Dra-nupC-pdp operon of Bacillus subtilis: nucleotide sequence, induction by deoxyribonucleosides, and transcriptional regulation by the deoR-encoded DeoR repressor protein. J Bacteriol. 1996; 178(2):424-34. PMC: 177674. DOI: 10.1128/jb.178.2.424-434.1996. View

Patching S, Baldwin S, Baldwin A, Young J, Gallagher M, Henderson P . The nucleoside transport proteins, NupC and NupG, from Escherichia coli: specific structural motifs necessary for the binding of ligands. Org Biomol Chem. 2005; 3(3):462-70. DOI: 10.1039/b414739a. View

McLaughlin S, Zhalnina K, Kosina S, Northen T, Sasse J . The core metabolome and root exudation dynamics of three phylogenetically distinct plant species. Nat Commun. 2023; 14(1):1649. PMC: 10039077. DOI: 10.1038/s41467-023-37164-x. View

10.

Schuch R, Garibian A, Saxild H, Piggot P, Nygaard P . Nucleosides as a carbon source in Bacillus subtilis: characterization of the drm-pupG operon. Microbiology (Reading). 1999; 145 ( Pt 10):2957-66. DOI: 10.1099/00221287-145-10-2957. View

11.

Pietrangelo T . Raising the Guanosine-Based Molecules as Regulators of Excitable Tissues by the Exosomal-Vehiculated Signaling. Front Pharmacol. 2021; 12:658370. PMC: 8363250. DOI: 10.3389/fphar.2021.658370. View

12.

Ortega A, Zhulin I, Krell T . Sensory Repertoire of Bacterial Chemoreceptors. Microbiol Mol Biol Rev. 2017; 81(4). PMC: 5706747. DOI: 10.1128/MMBR.00033-17. View

13.

Turgeman T, Ben Asher J, Roth-Bejerano N, Kagan-Zur V, Kapulnik Y, Sitrit Y . Mycorrhizal association between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum alters plant physiology and fitness to arid conditions. Mycorrhiza. 2011; 21(7):623-630. DOI: 10.1007/s00572-011-0369-z. View

14.

Schulz-Bohm K, Gerards S, Hundscheid M, Melenhorst J, de Boer W, Garbeva P . Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J. 2018; 12(5):1252-1262. PMC: 5931972. DOI: 10.1038/s41396-017-0035-3. View

15.

Tuteja N, Singh M, Misra M, Bhalla P, Tuteja R . Molecular mechanisms of DNA damage and repair: progress in plants. Crit Rev Biochem Mol Biol. 2001; 36(4):337-97. DOI: 10.1080/20014091074219. View

16.

Paul D, Singh R, Jain R . Chemotaxis of Ralstonia sp. SJ98 towards p-nitrophenol in soil. Environ Microbiol. 2006; 8(10):1797-804. DOI: 10.1111/j.1462-2920.2006.01064.x. View

17.

Akiyama K, Matsuzaki K, Hayashi H . Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005; 435(7043):824-7. DOI: 10.1038/nature03608. View

18.

Satish L, Barak H, Keren G, Yehezkel G, Kushmaro A, Ben-Dov E . The Microbiome Structure of the Symbiosis between the Desert Truffle and Its Host Plant . J Fungi (Basel). 2022; 8(10). PMC: 9605525. DOI: 10.3390/jof8101062. View

19.

Matilla M, Krell T . The effect of bacterial chemotaxis on host infection and pathogenicity. FEMS Microbiol Rev. 2017; 42(1). DOI: 10.1093/femsre/fux052. View

20.

DeLoney-Marino C, Wolfe A, Visick K . Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl Environ Microbiol. 2003; 69(12):7527-30. PMC: 310003. DOI: 10.1128/AEM.69.12.7527-7530.2003. View