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A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian-Symbiodiniaceae symbioses.

ABSTRACT: Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that despite their independent evolution, cnidarian hosts use the same carbon-nitrogen negative feedback loop to control symbiont proliferation. Symbiont-derived photosynthates are used to assimilate nitrogenous waste via glutamine synthetase-glutamate synthase-mediated amino acid biosynthesis in a carbon-dependent manner, which regulates the availability of nitrogen to the symbionts. Using nutrient supplementation experiments, we show that the provision of additional carbohydrates significantly reduces symbiont density while ammonium promotes symbiont proliferation. High-resolution metabolic analysis confirmed that all hosts co-incorporated glucose-derived ¹³C and ammonium-derived ¹⁵N via glutamine synthetase-glutamate synthase-mediated amino acid biosynthesis. Our results reveal a general carbon-nitrogen negative feedback loop underlying these symbioses and provide a parsimonious explanation for their repeated evolution.

SUBMITTER: Cui G

PROVIDER: S-EPMC10620218 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian-Symbiodiniaceae symbioses.

Cui Guoxin G Mi Jianing J Moret Alessandro A Menzies Jessica J Zhong Huawen H Li Angus A Hung Shiou-Han SH Al-Babili Salim S Aranda Manuel M

Nature communications 20231101 1

Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that despite their independent evolution, cnidarian hosts use the same carbon-nitrogen negative feedback loop to control symbiont proliferation. Symbiont-derived photosynthates are used to assimilate nitrogenous wa ...[more]

PMID: 37914686

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Project description:The nitrogen (N) status transduced via the NtrBC two-component system is a major signaling cue in the root nodule endosymbiosis of diazotrophic rhizobia with legumes. NtrBC is upregulated in the N-limiting rhizosphere environment at the onset of nodulation but silenced in nodules to favor the assimilation of the fixed N into plant biomass. We reported that the trans-acting sRNA NfeR1 (Nodule Formation Efficiency RNA) broadly influences the symbiotic performance of the α-rhizobium Sinorhizobium meliloti. Here, we show that NfeR1 is indeed an N-responsive sRNA that fine-tunes NtrBC output during the symbiotic transition. Biochemical and genetic approaches unveiled that NtrC and the LysR-type symbiotic regulator LsrB bind at distinct nearby sites in the NfeR1 promoter, acting antagonistically as repressor and activator of transcription, respectively. This complex transcriptional control specifies peak NfeR1 steady-state levels in N-starved and endosymbiotic bacteria. Furthermore, NfeR1 base pairs the translation initiation region of the histidine kinase coding mRNA ntrB, causing a decrease in both NtrB and NtrC abundance as assessed by double-plasmid genetic assays. In the context of endogenous regulation, NfeR1-mediated ntrBC silencing most likely amends the effective strength of the known operon autorepression exerted by NtrC. Accordingly, a lack of NfeR1 shifts the wild-type NtrBC output, restraining the fitness of free-living rhizobia under N stress and plant growth upon nodulation. The mixed NtrBC-NfeR1 double-negative feedback loop is thus an unprecedented adaptive network motif that helps α-rhizobia adjust N metabolism to the demands of an efficient symbiosis with legume plants. IMPORTANCE Root nodule endosymbioses between diazotrophic rhizobia and legumes provide the largest input of combined N to the biosphere, thus representing an alternative to harmful chemical fertilizers for sustainable crop production. Rhizobia have evolved intricate strategies to coordinate N assimilation for their own benefit with N2 fixation to sustain plant growth. The rhizobial N status is transduced by the NtrBC two-component system, the seemingly ubiquitous form of N signal transduction in Proteobacteria. Here, we show that the regulatory sRNA NfeR1 (nodule formation efficiency RNA) of the alfalfa symbiont Sinorhizobium meliloti is transcribed from a complex promoter repressed by NtrC in a N-dependent manner and feedback silences ntrBC by complementary base-pairing. These findings unveil a more prominent role of NtrC as a transcriptional repressor than hitherto anticipated and a novel RNA-based mechanism for NtrBC regulation. The NtrBC-NfeR1 double-negative feedback loop accurately rewires symbiotic S. meliloti N metabolism and is likely conserved in α-rhizobia.

Dataset Information

A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian-Symbiodiniaceae symbioses.

Publications

A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian-Symbiodiniaceae symbioses.

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