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Genetic, Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Implications

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Genetic, Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Implications G C A T T A C G G C A T genes Review Genetic, Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Implications Corinne Cassier-Chauvat , Victoire Blanc-Garin and Franck Chauvat * Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRS, 91198 Gif-sur-Yvette, France; [email protected] (C.C.-C.); [email protected] (V.B.-G.) * Correspondence: [email protected]; Tel.: +33-1-69-08-78-11 Abstract: Cyanobacteria are widely-diverse, environmentally crucial photosynthetic prokaryotes of great interests for basic and applied science. Work to date has focused mostly on the three non- nitrogen fixing unicellular species Synechocystis PCC 6803, Synechococcus PCC 7942, and Synechococcus PCC 7002, which have been selected for their genetic and physiological interests summarized in this review. Extensive “omics” data sets have been generated, and genome-scale models (GSM) have been developed for the rational engineering of these cyanobacteria for biotechnological purposes. We presently discuss what should be done to improve our understanding of the genotype-phenotype relationships of these models and generate robust and predictive models of their metabolism. Fur- thermore, we also emphasize that because Synechocystis PCC 6803, Synechococcus PCC 7942, and Synechococcus PCC 7002 represent only a limited part of the wide biodiversity of cyanobacteria, other species distantly related to these three models, should be studied. Finally, we highlight the need to strengthen the communication between academic researchers, who know well cyanobacteria and can engineer them for biotechnological purposes, but have a limited access to large photobioreactors, and Citation: Cassier-Chauvat, C.; industrial partners who attempt to use natural or engineered cyanobacteria to produce interesting Blanc-Garin, V.; Chauvat, F. Genetic, chemicals at reasonable costs, but may lack knowledge on cyanobacterial physiology and metabolism. Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Keywords: Synechocystis PCC 6803; Synechococcus PCC 7942; Synechococcus PCC 7002; biodiver- Implications. Genes 2021, 12, 500. sity; genotype-phenotype relationships; conjugation; transformation; RSF1010 plasmid; neutral https://doi.org/10.3390/ cloning sites genes12040500 Academic Editors: Denis Baurain and Luc Cornet 1. Introduction Received: 26 January 2021 Cyanobacteria are ancient Gram-negative prokaryotes that perform oxygenic photo- Accepted: 25 March 2021 synthesis and are phylogenetically close to recently discovered non-photosynthetic bacteria Published: 29 March 2021 termed Melainabacteria and Sericytochromatia [1,2]. Cyanobacteria are regarded as the producer of the atmospheric oxygen (O2) of Earth [3] and the ancestors of the plant chloro- Publisher’s Note: MDPI stays neutral plast [4]. Cyanobacteria capture solar energy at high efficiencies (3–9%) [5] to power up with regard to jurisdictional claims in their efficient photoautotrophic metabolism, which fixes huge amounts of inorganic carbon published maps and institutional affil- (CO2, NaHCO3, and Na2CO3) and nitrogen (N2, NH4, NO2, NO3, or urea) [6,7], into an iations. enormous biomass [8] that supports a large part of the food chain. By colonizing aquatic ecosystems (fresh, brackish, and marine waters) and soils (in- cluding deserts) of our planet, cyanobacteria are inevitably exposed to multiple stresses such as solar ultraviolet radiations and variations in light intensity and quality, inorganic- Copyright: © 2021 by the authors. nutrients availabilities, temperatures (high and low), salinity, pH (acidic and basic), drought, Licensee MDPI, Basel, Switzerland. and pollutants (herbicides and heavy-metals). In addition, cyanobacteria are involved in This article is an open access article numerous interactions with competitors, predators, or symbiotic hosts [9]. Consequently, it distributed under the terms and is not surprising that cyanobacteria have evolved as a widely diverse organisms, which are conditions of the Creative Commons of high interest for basic and applied research [10]. They display various metabolisms and Attribution (CC BY) license (https:// morphologies [11,12], and numerous species can differentiate cells, akinetes (spores) and/or creativecommons.org/licenses/by/ heterocysts, which are dedicated to growth or survival under adverse conditions [13,14]. 4.0/). Genes 2021, 12, 500. https://doi.org/10.3390/genes12040500 https://www.mdpi.com/journal/genes Genes 2021, 12, x FOR PEER REVIEW 2 of 43 metabolisms and morphologies [11,12], and numerous species can differentiate cells, Genes 2021, 12, 500 2 of 42 akinetes (spores) and/or heterocysts, which are dedicated to growth or survival under ad- verse conditions [13,14]. Thus, cyanobacteria are good model organisms to study the im- pact of environmental conditions on the physiology, metabolism, and morphology of mi- Thus,crobial cyanobacteria cells. Furthermore, are good cyanobacteria model organisms synthesize to study a wide the impact variety of of environmental bioactive metabo- con- ditionslites (Figure on the 1), physiology, many of which metabolism, being of and interest morphology for human of microbial health [15–18], cells. Furthermore,and they are cyanobacteriaregarded as promising synthesize cell a wide factories variety for of the bioactive production metabolites of chemicals (Figure1 ),(fuels many and of whichbiode- beinggradable of interest bioplastics) for human from healthhighly [ 15abundant–18], and natural they are resources: regarded assolar promising energy, cell water factories (not fornecessarily the production potable), of chemicalsCO2, and minerals, (fuels and thanks biodegradable to their active bioplastics) photosynthesis from highly and abundant the syn- naturalthetic biology resources: tools solar of model energy, species water [10,19,20]. (not necessarily potable), CO2, and minerals, thanks to their active photosynthesis and the synthetic biology tools of model species [10,19,20]. Figure 1. Cyanobacteria can synthesize a wealth of biotechnologically interesting products. Figure 1. Cyanobacteria can synthesize a wealth of biotechnologically interesting products. Most of our knowledge on cyanobacteria came from studying the three non-nitrogen fixing,Most unicellular of our knowledge cyanobacteria on cyanobacteriaSynechocystis PCC came 6803, fromSynechococcus studying thePCC three 7942 non-nitrogen (formerly namedfixing, unicellular “Anacystis nidulanscyanobacteria”) and SynechococcusSynechocystis PCC 70026803, (formerly Synechococcus named PCC “Agmenellum 7942 (for- quadruplicatummerly named “PR6”)Anacystis that nidulans” are (i) straightforward) and Synechococcus to culture PCCunder 7002 (formerly laboratory named conditions, “Agmen- (ii) amenableellum quadruplicatum to genetic manipulation, PR6”) that are and (i) straightforward (iii) freezable for to long-term culture under storage. laboratory In this review, condi- wetions, will (ii) summarize amenablethe to genetic andmanipulation, physiological and properties (iii) freezable of these for models,long-term emphasizing storage. In onthis their review, tolerance we will to summarize stresses, and the the genetic recent an progressd physiological in their properties genetics. Weof these will alsomodels, put forwardemphasizing that inon spite their of tolerance more than to three stresses, decades and ofthe intensive recent progress research thein their genomes genetics. of these We modelswill also still put contain forward a large that number in spite of of genes more and than small three RNAs decades (sRNAs) of intensive of unknown research function. the Furthermore,genomes of these many models of the still genes contain annotated a large number “by sequence of genes analogy” and small with RNAs those (sRNAs) genes characterizedof unknown function. in intensively Furthermore, studied, many non-photosynthetic, of the genes annotated models “by such sequence as Escherichia analogy” coli mightwith those in fact genes have characterized a different function in intensivel in cyanobacteria.y studied, Thisnon-photosynthetic, situation makes comparativemodels such genomicsas Escherichia and coli metabolic might in modeling fact have difficult. a different Consequently, function in wecyanobacteria. will discuss This that tosituation better understandmakes comparative and exploit genomics the wide and biodiversity metabolic of modeling cyanobacteria, difficult. strong Consequently, efforts should we be will put indiscuss large-scale that to analysis better ofunderstand genes and sRNAsand exploi functionst the wide in model biodiversity cyanobacteria. of cyanobacteria, Finally, we willstrong emphasize efforts should that we be need put in to large-scale identify and an thoroughlyalysis of genes study and new sRNAs cyanobacteria functions endowed in model withcyanobacteria. natural properties Finally, we of will interest emphasize for basic th orat we applied need researches,to identify and and thoroughly test whether study the synthetic biology tools developed for model strains can be used to facilitate the engineering of these newly identified cyanobacteria so as to turn their promises into industrial realities. Genes 2021, 12, 500 3 of 42 2. Cyanobacteria Being Inevitably Exposed to Photo-Oxidative Stress Have Developed the Evolutionary-Conserved Glutathione System Having evolved the oxygenic photosynthesis [21], cyanobacteria were the first or- 1 ganisms to be exposed to the toxic reactive oxygen
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