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Competition and interdependence: The multifaceted interaction of symbiotic Nostoc sp. and Agrobacterium sp. under inorganic carbon limitation

ABSTRACT: Nostoc cyanobacteria are capable to form symbiotic relationships with plants, transitioning to a heterotrophic lifestyle in return for providing bioavailable nitrogen to the host. The diazotrophic photoautotrophs also serve as a hub for a specialized heterotrophic bacterial community whose physiological contributions are poorly understood. By comparing the axenic strain N. punctiforme PCC 73102 and the related strains Nostoc sp. KVJ2 and KVJ3, which still maintain their heterotrophic microbiome, we were able to demonstrate an almost obligate dependence of the cyanobacteria on the heterotrophic partners under carbon-limiting conditions. Detailed analysis of the intimate bilateral relationship between Nostoc punctiforme and the isolate Agrobacterium tumefaciens Het4 using multi-omics technologies and microscopy uncovered a complex partnership characterized, among other traits, by competition for iron and facilitation for carbon. Although competitive interactions with A. tumefaciens Het4 compromise nitrogen fixation and stimulate the degradation of cyanophycin, mutualistic dependency prevails under inorganic carbon limitation. Both the absence of the high affinity bicarbonate uptake transporter SbtA and the prevalent extracarboxysomal localization of the carbon-fixing enzyme RubisCO as detected by immunofluorescence microscopy suggest a weak carbon concentrating mechanism in N. punctiforme that enforces a dependence on heterotrophic bacteria. Further, immunofluorescence, electron microscopic and proteomic analyses reveal a pronounced extracellular recycling of proteins under N- and C-limiting conditions. The pivotal influence of heterotrophic bacteria on symbiotic Nostoc strains should be considered when analyzing these strains, especially in the free-living state, and also sheds new light on the benefit to Nostoc of the provision of organic carbon by plant hosts.

INSTRUMENT(S): Bruker Daltonics timsTOF series

ORGANISM(S): Nostoc Punctiforme (strain Atcc 29133 / Pcc 73102)

SUBMITTER: David A. Russo

LAB HEAD: David A. Russo

PROVIDER: PXD052511 | Pride | 2025-04-09

REPOSITORIES: Pride

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Project description:The trophic condition related proteomes of an oxygenic photosynthetic cyanobacterium Synechocystis sp. PCC 6803 (glucose tolerant strain) were analyzed to get further insights into the metabolic traits governing the early exponential growth under photoautotrophic, mixotrophic and heterotrophic conditions. The cells were grown under constant light autotrophically (AT) in low (air-level) CO2 (ATLC) and in high CO2 (ATHC), mixotrophically (MT) in low (air-level) CO2 in the presence of glucose (MTLC) and heterotrophically in low (air-level) CO2 in the presence of glucose and only 10 min exposure to light every 24 hours (Light-Activated Heterotrophic Growth; LAHGLC). The proteomes of ATHC, MTLC and LAHGLC differed substantially from that of ATLC, particularly by downregulation of the inducible carbon concentrating mechanisms (CCM) and photorespiration related enzymes. On the contrary, under carbon-rich conditions (ATHC, MTLC, LAHGLC) the cells accumulated respiratory NAD(P)H dehydrogenase I complexes in the thylakoid membrane. In glucose supplemented cultures (MTLC, LAHGLC) a distinct NDH-2 protein, NdbA, additionally accumulated in the thylakoid membrane whilst the plasma membrane localized NdbC and ARTO decreased in abundance. The light-harvesting proteins together with the photosystem I and II subunits were uniquely depleted under LAHGLC condition, accumulated under ATHC and in MTLC remained at the level of the reference ATLC condition. The accumulation of P-transporters was unique, revealing only minor differences between ATLC and ATHC but strong up-regulation in MTLC and down-regulation in LAHGLC. This likely implies that MTLC stores energy surplus in the highly energetic bonds of polyphosphate polymer that can be used under unfavorable growth conditions. It is concluded that the rigor of cell growth in MTLC condition results to a great extent from high intracellular inorganic carbon conditions created upon glucose breakdown and release of CO2, beside the direct utilization of glucose-derived carbon skeletons for growth. This combination provides the MTLC cultures with excellent conditions for growth that often exceeds that of the mere photoautotrophic growth at high CO2.

Project description:Every cyanobacterial species contains gene encoding site-2-protease (S2P) homolog. The studied prokaryotic S2P homologs play essential roles in regulating stress response through intramembrane proteolysis of membrane-bound anti-sigma factors. Here, gene of Slr0643, one of four S2P homologs in Synechocystis sp. PCC 6803, was insertionally disrupted to explore its physiological role. Only a partially segregated mutant was obtained, indicating its indispensability for growth. The partially disrupted mutant could not grow at pH 6.5, while wild type acclimated to pH 6.5 quickly. The slr0643 gene expression was transiently induced after pH transfer from 7.5 to 6.5. Both evidences demonstrated the pivotal role of fully functional Slr0643 in acid acclimation. DNA microarray and quantitative RT-PCR analyses decoded genes involved in early acid acclimation and revealed differentially expressed genes due to slr0643 disruption at both pH conditions. Early acid acclimation to pH 6.5 included upregulation of sigH, hik16 and hik35, and downregulation of pcrR and sigG; as well as downregulation of porins and upregulation of inorganic carbon and nitrogen transporters. Defective photosynthesis and excess expression of NADH dehydrogenase, together with over upregulation of carbon transporter and repression of nitrogen transporter and metabolism gene contributed to the acid lethality of mutant at pH 6.5. Most interestingly, analysis of microarray data revealed the close relationship between slr0643 disruption and expression of sigH operon. Therefore it was implied that Slr0643/Sll0857/SigH might acts through S2P/anti-Sigma factor/Sigma factor mechanism to play a role in acid acclimation. M-bM-^@M-^C Loop design was used to compare differential expression of wild type and mutant at pH 7.5 and pH 6.5 respectively, including dye-swape. Biological variation was sampled by extracting RNA from three independent experiments and pooling them together before hybridizations. Two or four replicate chips for each comparison and two replicate printings per chip represent technical repeats.

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Competition and interdependence: The multifaceted interaction of symbiotic Nostoc sp. and Agrobacterium sp. under inorganic carbon limitation

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