Oxidative‐stress detoxification and signalling in cyanobacteria: the crucial glutathione synthesis pathway supports the production of ergothioneine and ophthalmate

Narainsamy, Kinsley; Farci, Sandrine; Braun, Emilie; Junot, Christophe; Cassier‐Chauvat, Corinne; Chauvat, Franck

doi:10.1111/mmi.13296

Cited by 56 publications

(55 citation statements)

References 40 publications

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“…Cyanobacteria produce a wealth of natural products that can influence human health (antioxidants, vitamins, antibacterial, toxins (Williams, 2009; Dittmann et al, 2015; Kleigrewe et al, 2016; Narainsamy et al, 2016). Hence, Arthrospira has served as a human food since time immemorial (Gao, 1998).…”

Section: Introductionmentioning

confidence: 99%

Comparative Genomics of DNA Recombination and Repair in Cyanobacteria: Biotechnological Implications

2016

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Cyanobacteria are fascinating photosynthetic prokaryotes that are regarded as the ancestors of the plant chloroplast; the purveyors of oxygen and biomass for the food chain; and promising cell factories for an environmentally friendly production of chemicals. In colonizing most waters and soils of our planet, cyanobacteria are inevitably challenged by environmental stresses that generate DNA damages. Furthermore, many strains engineered for biotechnological purposes can use DNA recombination to stop synthesizing the biotechnological product. Hence, it is important to study DNA recombination and repair in cyanobacteria for both basic and applied research. This review reports what is known in a few widely studied model cyanobacteria and what can be inferred by mining the sequenced genomes of morphologically and physiologically diverse strains. We show that cyanobacteria possess many E. coli-like DNA recombination and repair genes, and possibly other genes not yet identified. E. coli-homolog genes are unevenly distributed in cyanobacteria, in agreement with their wide genome diversity. Many genes are extremely well conserved in cyanobacteria (mutMS, radA, recA, recFO, recG, recN, ruvABC, ssb, and uvrABCD), even in small genomes, suggesting that they encode the core DNA repair process. In addition to these core genes, the marine Prochlorococcus and Synechococcus strains harbor recBCD (DNA recombination), umuCD (mutational DNA replication), as well as the key SOS genes lexA (regulation of the SOS system) and sulA (postponing of cell division until completion of DNA reparation). Hence, these strains could possess an E. coli-type SOS system. In contrast, several cyanobacteria endowed with larger genomes lack typical SOS genes. For examples, the two studied Gloeobacter strains lack alkB, lexA, and sulA; and Synechococcus PCC7942 has neither lexA nor recCD. Furthermore, the Synechocystis PCC6803 lexA product does not regulate DNA repair genes. Collectively, these findings indicate that not all cyanobacteria have an E. coli-type SOS system. Also interestingly, several cyanobacteria possess multiple copies of E. coli-like DNA repair genes, such as Acaryochloris marina MBIC11017 (2 alkB, 3 ogt, 7 recA, 3 recD, 2 ssb, 3 umuC, 4 umuD, and 8 xerC), Cyanothece ATCC51142 (2 lexA and 4 ruvC), and Nostoc PCC7120 (2 ssb and 3 xerC).

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Section: Introductionmentioning

confidence: 99%

Comparative Genomics of DNA Recombination and Repair in Cyanobacteria: Biotechnological Implications

2016

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“…; Narainsamy et al . ). Ophthalmic acid was initially discovered in calf lens (Waley ), but its physiological function is not understood.…”

Section: Resultsmentioning

confidence: 97%

Diverse fission yeast genes required for responding to oxidative and metal stress: Comparative analysis of glutathione‐related and other defense gene deletions

et al. 2016

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Living organisms have evolved multiple sophisticated mechanisms to deal with reactive oxygen species. We constructed a collection of twelve single-gene deletion strains of the fission yeast Schizosaccharomyces pombe designed for the study of oxidative and heavy metal stress responses. This collection contains deletions of biosynthetic enzymes of glutathione (Dgcs1 and Dgsa1), phytochelatin (Dpcs2), ubiquinone (Dabc1) and ergothioneine (Degt1), as well as catalase (Dctt1), thioredoxins (Dtrx1 and Dtrx2), Cu/Zn-and Mn-superoxide dismutases (SODs; Dsod1 and Dsod2), sulfiredoxin (Dsrx1) and sulfide-quinone oxidoreductase (Dhmt2). First, we employed metabolomic analysis to examine the mutants of the glutathione biosynthetic pathway. We found that ophthalmic acid was produced by the same enzymes as glutathione in S. pombe. The identical genetic background of the strains allowed us to assess the severity of the individual gene knockouts by treating the deletion strains with oxidative agents. Among other results, we found that glutathione deletion strains were not particularly sensitive to peroxide or superoxide, but highly sensitive to cadmium stress. Our results show the astonishing diversity in cellular adaptation mechanisms to various types of oxidative and metal stress and provide a useful tool for further research into stress responses.

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“…-genes involved in cyanobacterial GSH synthesis (gshA an gshB) and GSH catabolism (ggt) (Narainsamy et al, 2016); gpx1 and gpx2 orthologues to human GPX4, which is essential for ferroptosis in animals (Friedmann Angeli et al, 2014;Imai et al, 2017). Three genes, gshA, ggt and gpx2 were up-regulated after 50ºC exposure and only gpx2 was down-regulated.…”

Section: Molecular Mechanisms Governing Ferroptosis In Synechocystismentioning

confidence: 99%

Heat stress induces ferroptosis in a photosynthetic prokaryote

Aguilera

Berdun

Bártoli

et al. 2019

Preprint

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Aguilera et al, show that ferroptosis, an oxidative and iron-dependent form of regulated cell death, plays an important role in the cyanobacterium Synechocystis sp.PCC 6803 in response to heat stress. AbstractFerroptosis is an oxidative and iron-dependent form of regulated cell death (RCD) recently described in eukaryotic organisms like animals, plants and parasites.Here we report that a similar process takes place in the photosynthetic prokaryote Synechocystis sp. PCC 6803 in response to heat stress. After a heat shock, Synechocystis PCC 6803 cells undergo a cell death pathway that can be suppressed by the canonical ferroptosis inhibitors, CPX or Fer-1, or by external addition of calcium (Ca ++ ), glutathione (GSH) or ascorbic acid (AsA). Moreover, as described for eukaryotic cells ferroptosis, this pathway is characterized by an early depletion of the antioxidants GSH and AsA, and by lipid peroxidation. In general, prokaryotes membranes contain poorly oxidizable saturated or monounsaturated lipid molecules, it was thought that free prokaryotes were not susceptible to ferroptosis but interestingly, that is not the case of cyanobacteria, which contain thylakoid membranes that are enriched in polyunsaturated-fatty-acid-containing phospholipids. These results indicate that all of the hallmarks described for eukaryotic ferroptosis are conserved in photosynthetic prokaryotes and suggest that ferroptosis might be an ancient cell death program.

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Oxidative‐stress detoxification and signalling in cyanobacteria: the crucial glutathione synthesis pathway supports the production of ergothioneine and ophthalmate

Cited by 56 publications

References 40 publications

Comparative Genomics of DNA Recombination and Repair in Cyanobacteria: Biotechnological Implications

Comparative Genomics of DNA Recombination and Repair in Cyanobacteria: Biotechnological Implications

Diverse fission yeast genes required for responding to oxidative and metal stress: Comparative analysis of glutathione‐related and other defense gene deletions

Heat stress induces ferroptosis in a photosynthetic prokaryote

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