Host-dependent specialized metabolism of nitrogen export in actinorhizal nodules induced by diazotrophic Actinomycetota Frankia cluster-2

Abstract

Frankia cluster-2 strains are diazotrophs that engage in root nodule symbiosis with actinorhizal plants of the Cucurbitales and the Rosales. Previous studies have shown that an assimilated nitrogen source, presumably arginine, is exported to the host in nodules of Datisca glomerata (Cucurbitales), while a different metabolite is exported in the nodules of Ceanothus thyrsiflorus (Rosales). To investigate if an assimilated nitrogen form is commonly exported to the host by cluster-2 strains, and which metabolite would be exported in Ceanothus, we analysed gene expression levels, metabolite profiles, and enzyme activities in nodules. We conclude that the export of assimilated nitrogen in symbiosis seems to be a common feature for Frankia cluster-2 strains, but the source of nitrogen is host dependent. The export of assimilated ammonium to the host suggests that 2-oxoglutarate is drawn from the tricarboxylic acid (TCA) cycle at a high rate. This specialized metabolism obviates the need for the reductive branch of the TCA cycle. We found that several genes encoding enzymes of central carbon and nitrogen metabolism were lacking in Frankia cluster-2 genomes: the glyoxylate shunt and succinate semialdehyde dehydrogenase. This led to a linearization of the TCA cycle, and we hypothesized that this could explain the low saprotrophic potential of Frankia cluster-2.Frankia cluster-2 shows several gene losses related to the tricarboxylic acid cycle. We have hypothesized that this is associated with their specialized metabolism, and exchange of nutrients, during root nodule symbiosis.

Keywords

Actinorhizal symbiosis; Frankia; GS synthetase; nitrogenase; root nodules; succinic semialdehyde dehydrogenase; TCA cycle

Published in

Journal of Experimental Botany
2024
Publisher: OXFORD UNIV PRESS

SLU Authors

• Berckx, Fede

  • Department of Crop Production Ecology, Swedish University of Agricultural Sciences
    
  • Stockholm University

UKÄ Subject classification

Botany

Publication identifier

• DOI: https://doi.org/10.1093/jxb/erae446

Permanent link to this page (URI)

https://res.slu.se/id/publ/139881