Homospermidine biosynthesis in the cyanobacterium <i>Anabaena</i> requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth

Burnat, Mireia; Li, Bin; Kim, Sok Ho; Michael, Anthony J.; Flores, Enrique

doi:10.1111/mmi.14006

Cited by 26 publications

(39 citation statements)

References 56 publications

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“…We have recently described a pathway producing sym ‐homospermidine from arginine in Anabaena (Burnat et al , ). The first enzyme in this pathway is arginine decarboxylase encoded by speA ( all3401 ), and an speA mutant is drastically hampered in diazotrophic growth apparently because of a requirement for polyamines during heterocyst differentiation (Burnat et al , ). Here, we studied the growth rate constants of the agrE and putA mutants in liquid medium.…”

Section: Resultsmentioning

confidence: 99%

“…Our work has identified in the heterocyst-forming cyanobacterium Anabaena an arginine catabolism pathway that produces glutamate mediated by the products of only two genes, agrE (alr4995 in the Anabaena genome) and putA (alr0540). Figure 10 depicts this pathway along with the homospermidine biosynthesis pathway that we have recently described in Anabaena (Burnat et al, 2018). Among the pathways that catabolize arginine producing glutamate and ammonium, the use of ornithine as an intermediate is common.…”

Section: Discussionmentioning

confidence: 99%

“…ORF all3401 ( speA ) encodes arginine decarboxylase, and the arginine decarboxylase deletion mutant (∆ speA ::C.S3) has been described previously (Burnat et al , ). To create a double ∆ agrE ∆ speA ::C.S3 mutant, plasmid constructs used to create the speA mutant were transferred to Anabaena ∆ agrE by triparental mating, as described above, with selection for Sm R Sp R .…”

Section: Methodsmentioning

confidence: 99%

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Catabolic pathway of arginine in Anabaena involves a novel bifunctional enzyme that produces proline from arginine

Burnat

Picossi

Valladares

et al. 2019

Molecular Microbiology

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Summary Arginine participates widely in metabolic processes. The heterocyst‐forming cyanobacterium Anabaena catabolizes arginine to produce proline and glutamate, with concomitant release of ammonium, as major products. Analysis of mutant Anabaena strains showed that this catabolic pathway is the product of two genes, agrE (alr4995) and putA (alr0540). The predicted PutA protein is a conventional, bifunctional proline oxidase that produces glutamate from proline. In contrast, AgrE is a hitherto unrecognized enzyme that contains both an N‐terminal α/β propeller domain and a unique C‐terminal domain of previously unidentified function. In vitro analysis of the proteins expressed in Escherichia coli or Anabaena showed arginine dihydrolase activity of the N‐terminal domain and ornithine cyclodeaminase activity of the C‐terminal domain, overall producing proline from arginine. In the diazotrophic filaments of Anabaena, β‐aspartyl‐arginine dipeptide is transferred from the heterocysts to the vegetative cells, where it is cleaved producing aspartate and arginine. Both agrE and putA were found to be expressed at higher levels in vegetative cells than in heterocysts, implying that arginine is catabolized by the AgrE‐PutA pathway mainly in the vegetative cells. Expression in Anabaena of a homolog of the C‐terminal domain of AgrE obtained from Methanococcus maripaludis enabled us to identify an archaeal ornithine cyclodeaminase.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Catabolic pathway of arginine in Anabaena involves a novel bifunctional enzyme that produces proline from arginine

Burnat

Picossi

Valladares

et al. 2019

Molecular Microbiology

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“…Although the mechanisms of assimilation of organic N have not been investigated in detail, some relevant pathways can be predicted or have been approached experimentally. Thus, (i) glutamine utilization likely involves GOGAT (described above); (ii) arginine utilization appears to take place through two pathways, including an arginine decarboxylase pathway that synthesizes polyamines (Burnat et al ., ) and an arginine ➔ proline ➔ glutamate pathway (Burnat and Flores, ) and (iii) urea utilization involves urease that hydrolyzes urea to CO 2 and two molecules of ammonium (Valladares et al ., ).…”

Section: Assimilation Of Combined N Sources Alternative To Ammoniummentioning

confidence: 99%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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Heterocyst-forming cyanobacteria are filamentous organisms that perform oxygenic photosynthesis and CO fixation in vegetative cells and nitrogen fixation in heterocysts, which are formed under deprivation of combined nitrogen. These organisms can acclimate to use different sources of nitrogen and respond to different levels of CO . Following work mainly done with the best studied heterocyst-forming cyanobacterium, Anabaena, here we summarize the mechanisms of assimilation of ammonium, nitrate, urea and N , the latter involving heterocyst differentiation, and describe aspects of CO assimilation that involves a carbon concentration mechanism. These processes are subjected to regulation establishing a hierarchy in the assimilation of nitrogen sources -with preference for the most reduced nitrogen forms- and a dependence on sufficient carbon. This regulation largely takes place at the level of gene expression and is exerted by a variety of transcription factors, including global and pathway-specific transcriptional regulators. NtcA is a CRP-family protein that adjusts global gene expression in response to the C-to-N balance in the cells, and PacR is a LysR-family transcriptional regulator (LTTR) that extensively acclimates the cells to oxygenic phototrophy. A cyanobacterial-specific transcription factor, HetR, is involved in heterocyst differentiation, and other LTTR factors are specifically involved in nitrate and CO assimilation.

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“…These two amino acids, especially the nitrogen-rich arginine, must be catabolized to make their nitrogen atoms available for cyanobacterial metabolism. Arginine can be used for synthesis of cyanophycin and serve as a precursor for synthesis of biomass components (protein) and polyamines (putrescine, spermidine and spermine) (Cunin et al, 1986;Schriek et al, 2007;Burnat, Li et al, 2018). Thus arginine metabolism plays a key role in nitrogen storage and mobilization in cyanobacteria.…”

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confidence: 99%

Arginine and nitrogen mobilization in cyanobacteria

Zhang

Yang

2019

Molecular Microbiology

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Summary Cyanobacteria have evolved mechanisms to adapt to environmental stress and nutrient availability, including accumulation of storage compounds in inclusions and granules. As arginine is a key building block of cyanophycin, a dynamic nitrogen reservoir in many cyanobacteria, arginine metabolism plays a key role in cyanobacterial nitrogen storage and remobilization. Recently, an arginine dihydrolase AgrE/ArgZ was identified as a major arginine‐degrading enzyme in nondiazotrophic Synechocystis, which catalyzes the conversion of arginine into ornithine and ammonia. The N‐terminal domain of AgrE/ArgZ is responsible for arginine dihydrolase activity. Burnat et al. (2019) identified the arginine catabolic pathway in diazotrophic Anabaena, which starts with the reaction catalyzed by AgrE/ArgZ. Moreover, this study identified the C‐terminal domain of AgrE/ArgZ as an ornithine cyclodeaminase that catalyze the conversion of ornithine to proline. The results demonstrated that arginine is catabolized to generate glutamate by the concerted action of AgrE/ArgZ and bifunctional proline oxidase PutA in the vegetative cells of Anabaena. These findings expand our knowledge on nitrogen mobilization and redistribution in Anabaena under nitrogen‐fixation conditions. AgrE/ArgZ is widely present in many diazotrophic cyanobacteria and may be important for their contribution to marine nitrogen fixation. AgrE/ArgZ may have potential applications in metabolic engineering and biotechnology.

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Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth

Cited by 26 publications

References 56 publications

Catabolic pathway of arginine in Anabaena involves a novel bifunctional enzyme that produces proline from arginine

Catabolic pathway of arginine in Anabaena involves a novel bifunctional enzyme that produces proline from arginine

Genetic responses to carbon and nitrogen availability in Anabaena

Arginine and nitrogen mobilization in cyanobacteria

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