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A guanidine-degrading enzyme controls genomic stability of ethylene-producing cyanobacteria.

ABSTRACT: Recent studies have revealed the prevalence and biological significance of guanidine metabolism in nature. However, the metabolic pathways used by microbes to degrade guanidine or mitigate its toxicity have not been widely studied. Here, via comparative proteomics and subsequent experimental validation, we demonstrate that Sll1077, previously annotated as an agmatinase enzyme in the model cyanobacterium Synechocystis sp. PCC 6803, is more likely a guanidinase as it can break down guanidine rather than agmatine into urea and ammonium. The model cyanobacterium Synechococcus elongatus PCC 7942 strain engineered to express the bacterial ethylene-forming enzyme (EFE) exhibits unstable ethylene production due to toxicity and genomic instability induced by accumulation of the EFE-byproduct guanidine. Co-expression of EFE and Sll1077 significantly enhances genomic stability and enables the resulting strain to achieve sustained high-level ethylene production. These findings expand our knowledge of natural guanidine degradation pathways and demonstrate their biotechnological application to support ethylene bioproduction.

SUBMITTER: Wang B

PROVIDER: S-EPMC8390497 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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A guanidine-degrading enzyme controls genomic stability of ethylene-producing cyanobacteria.

Wang Bo B Xu Yao Y Wang Xin X Yuan Joshua S JS Johnson Carl H CH Young Jamey D JD Yu Jianping J

Nature communications 20210826 1

Recent studies have revealed the prevalence and biological significance of guanidine metabolism in nature. However, the metabolic pathways used by microbes to degrade guanidine or mitigate its toxicity have not been widely studied. Here, via comparative proteomics and subsequent experimental validation, we demonstrate that Sll1077, previously annotated as an agmatinase enzyme in the model cyanobacterium Synechocystis sp. PCC 6803, is more likely a guanidinase as it can break down guanidine rathe ...[more]

PMID: 34446715

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Project description:Ethylene is a gas that has long been known to act as a plant hormone. We recently showed that a cyanobacterium, Synechocystis sp. PCC 6803 (Synechocystis) contains an ethylene receptor (SynEtr1) that regulates cell surface and extracellular components leading to altered phototaxis and biofilm formation. To determine whether other cyanobacteria respond to ethylene, we examined the effects of exogenous ethylene on phototaxis of the filamentous cyanobacterium, Geitlerinema sp. PCC 7105 (Geitlerinema). A search of the Geitlerinema genome suggests that two genes encode proteins that contain an ethylene binding domain and Geitlerinema cells have previously been shown to bind ethylene. We call these genes GeiEtr1 and GeiEtr2 and show that in air both are expressed. Treatment with ethylene decreases the abundance of GeiEtr1 transcripts. Treatment of Geitlerinema with 1000 nL L-1 ethylene affected the phototaxis response to white light as well as monochromatic red light, but not blue or green light. This is in contrast to Synechocystis where we previously found ethylene affected phototaxis to all three colors. We also demonstrate that application of ethylene down to 8 nL L-1 stimulates phototaxis of both cyanobacteria as well as biofilm formation of Synechocystis. We formerly demonstrated that the transcript levels of slr1214 and CsiR1 in Synechocystis are reduced by treatment with 1000 nL L-1 ethylene. Here we show that application of ethylene down to 1 nL L-1 causes a reduction in CsiR1 abundance. This is below the threshold for most ethylene responses documented in plants. By contrast, slr1214 is unaffected by this low level of ethylene and only shows a reduction in transcript abundance at the highest ethylene level used. Thus, cyanobacteria are very sensitive to ethylene. However, the dose-binding characteristics of ethylene binding to Geitlerinema and Synechocystis cells as well as to the ethylene binding domain of SynEtr1 heterologously expressed in yeast, are similar to what has been reported for plants and exogenously expressed ethylene receptors from plants. These data are consistent with a model where signal amplification is occurring at the level of the receptors.

Project description:AbstractFilamentous cyanobacteria originate toxic harmful algal blooms (HABs) in aquatic ecosystems, severely impacting freshwater ecosystems and life. Despite being natural bloomers, these microorganisms are challenging to handle in vitro, due to the formation of aggregates with entangled filaments. Consequently, their precise growth dynamics, although vital to timely predict HABs, remains inaccessible. Here, we precisely assessed growth of the HAB forming cyanobacteria Oscillatoria nigroviridis, by cultivating filament suspensions in transparent, gas permeable, and portable fluoropolymer microcapillary strips. Direct optical observation of O. nigroviridis growth revealed shorter filaments comprising less than 50 cells grew at a slower rate, dN/dt = 0.09 cell/day compared to filaments comprising more than 50 cells, with dN/dt up to 0.47 cell/day. The fourfold increase in dN/dt is suggested as part of the blooming strategy of the microorganism. This work suggests that fluoropolymer microcapillary strips can be used for effortless sampling and high-resolution monitoring of HABs.Impact statementClimate change is increasing the occurrence of episodes of harmful algal bloom, where uncontrolled growth of noxious cyanobacteria such as Oscillatoria species has detrimental outcomes in both the environment and biomass production industry, consequently, impairing human and animal health due to the production of toxic or bioactive compounds. In particular, the study of growth dynamics of Oscillatoria species has been limited to unprecise methods due to complications with aliquoting filamentous biomass. Fluoropolymer microcapillary strips provide an ideal miniaturized platform for sampling, cultivation, and growth monitoring of O. nigroviridis strain UHCC 0327, which paves the way to foster better water quality management tools.Graphical abstractSupplementary informationThe online version contains supplementary material available at 10.1557/s43577-024-00813-7.

Project description:BackgroundIn Drosophila embryos, checkpoints maintain genome stability by delaying cell cycle progression that allows time for damage repair or to complete DNA synthesis. Drosophila MOF, a member of MYST histone acetyl transferase is an essential component of male X hyperactivation process. Until recently its involvement in G2/M cell cycle arrest and defects in ionizing radiation induced DNA damage pathways was not well established.ResultsDrosophila MOF is highly expressed during early embryogenesis. In the present study we show that haplo-insufficiency of maternal MOF leads to spontaneous mitotic defects like mitotic asynchrony, mitotic catastrophe and chromatid bridges in the syncytial embryos. Such abnormal nuclei are eliminated and digested in the yolk tissues by nuclear fall out mechanism. MOF negatively regulates Drosophila checkpoint kinase 2 tumor suppressor homologue. In response to DNA damage the checkpoint gene Chk2 (Drosophila mnk) is activated in the mof mutants, there by causing centrosomal inactivation suggesting its role in response to genotoxic stress. A drastic decrease in the fall out nuclei in the syncytial embryos derived from mof¹/+; mnkp⁶/+ females further confirms the role of DNA damage response gene Chk2 to ensure the removal of abnormal nuclei from the embryonic precursor pool and maintain genome stability. The fact that mof mutants undergo DNA damage has been further elucidated by the increased number of single and double stranded DNA breaks.Conclusionmof mutants exhibited genomic instability as evidenced by the occurance of frequent mitotic bridges in anaphase, asynchronous nuclear divisions, disruption of cytoskeleton, inactivation of centrosomes finally leading to DNA damage. Our findings are consistent to what has been reported earlier in mammals that; reduced levels of MOF resulted in increased genomic instability while total loss resulted in lethality. The study can be further extended using Drosophila as model system and carry out the interaction of MOF with the known components of the DNA damage pathway.

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A guanidine-degrading enzyme controls genomic stability of ethylene-producing cyanobacteria.

Publications

A guanidine-degrading enzyme controls genomic stability of ethylene-producing cyanobacteria.

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