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Molecular and Cellular Mechanisms Underlying the Microbial Survival Strategies: Insights into Temperature and Nitrogen Adaptations

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Climate Change and the Microbiome

Part of the book series: Soil Biology ((SOILBIOL,volume 63))

Abstract

Bacteria inhabit almost all ecological niches, including harsh environments of desert, oceans, hypersaline, volcanic and thermal biospheres, representing therefore one of the quantitatively most abundant organisms on earth. To survive under such a variety of ecological habitats, bacteria developed a number of strategies to rapidly adapt and respond to environmental changes by tuning down their metabolic activities, thus overcoming periods of unfavorable growth conditions. Generally, the processes of entering into and exiting from the metabolic stand-by mode are tightly regulated and characterized by a series of signaling events involving various secondary messenger molecules, signaling proteins, and regulatory RNAs. For example, the availability of nitrogen is highly variable in nature and, hence, considered as the limiting factor of microbial growth and development. Therefore, the nitrogen assimilation reactions require a tight regulation and a constant sensing of the quantity and quality of the available nitrogen. Temperature sensing is also essential for microbial survival. Consistently, microbes have developed diverse molecular strategies to sense temperature fluctuations and readjust their metabolism to survive and resume growth at a different temperature. In this chapter, we summarize the recent advances in our understanding of the microbial adaptation strategies toward environmental changes, specifically those related to temperature fluctuations and changes in nitrogen availability.

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References

  • Abatenh E, Gizaw B, Tsegaye Z, Tefera G (2018) Microbial function on climate change - a review. Environ Pollut Climate Change 2:1000147

    Article  Google Scholar 

  • Abduljalil JM (2018) Bacterial riboswitches and RNA thermometers: nature and contributions to pathogenesis. Non-coding RNA Res 3:54–63

    Article  CAS  Google Scholar 

  • Agostoni M, Montgomery BL (2014) Survival strategies in the aquatic and terrestrial world: the impact of second messengers on cyanobacterial processes. Life (Basel, Switzerland) 4(4):745–769. https://doi.org/10.3390/life4040745

    Article  Google Scholar 

  • Allen MM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae. Archiv fur Mikrobiologie 69(2):114–120. https://doi.org/10.1007/bf00409755

    Article  CAS  PubMed  Google Scholar 

  • Allen JF, Thake B, Martin WF (2019) Nitrogenase inhibition limited oxygenation of Earth’s proterozoic atmosphere. Trends Plant Sci 24:1022–1031

    Article  CAS  PubMed  Google Scholar 

  • Angilletta MJ, Huey RB, Frazier MR (2010) Thermodynamic effects on organismal performance: is hotter better? Physiol Biochem Zool 83:197–206

    Article  PubMed  Google Scholar 

  • Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814

    Article  CAS  PubMed  Google Scholar 

  • Beere HM (2004) ‘The stress of dying’: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117:2641–2651

    Article  CAS  PubMed  Google Scholar 

  • Bergersen FJ, Appleby CA (1981) Leghaemoglobin within bacteroid-enclosing membrane envelopes from soybean root nodules. Planta 152:534–543

    Article  CAS  PubMed  Google Scholar 

  • Bolay P, Muro-Pastor MI, Florencio FJ, Klahn S (2018) The distinctive regulation of cyanobacterial glutamine synthetase. Life (Basel) 8:52

    CAS  Google Scholar 

  • Bothe H, Schmitz O, Yates MG, Newton WE (2010) Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev 74:529–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol 4:333

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown JR, Masuchi Y, Robb FT, Doolittle WF (1994) Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J Mol Evol 38:566–576

    Article  CAS  PubMed  Google Scholar 

  • Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, Agostini F, Tartaglia GG, Hayer-Hartl M, Hartl FU (2012) DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1:251–264

    Article  CAS  PubMed  Google Scholar 

  • Cavicchioli R et al (2019) Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17:569–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chowdhury S, Maris C, Allain FHT, Narberhaus F (2006) Molecular basis for temperature sensing by an RNA thermometer. EMBO J 25:2487–2497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cimdins A, Klinkert B, Aschke-Sonnenborn U, Kaiser FM, Kortmann J, Narberhaus F (2014) Translational control of small heat shock genes in mesophilic and thermophilic cyanobacteria by RNA thermometers. RNA Biol 11:594–608

    Article  PubMed  PubMed Central  Google Scholar 

  • Commichau FM, Forchhammer K, Stülke J (2006) Regulatory links between carbon and nitrogen metabolism. Curr Opin Microbiol 9:167–172

    Article  CAS  PubMed  Google Scholar 

  • Cronan CS (2018) Microbial biogeochemistry. In: Ecosystem biogeochemistry: element cycling in the forest landscape. Springer, Cham, pp 31–40

    Chapter  Google Scholar 

  • Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci U S A 108:10591–10596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci U S A 105:6668–6672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Docherty KM, Gutknecht JLM (2012) The role of environmental microorganisms in ecosystem responses to global change: current state of research and future outlooks. Biogeochemistry 109:1–6

    Article  Google Scholar 

  • Doello S et al (2018) A specific glycogen mobilization strategy enables rapid awakening of dormant cyanobacteria from chlorosis. Plant Physiol 177:594–603. https://doi.org/10.1104/pp.18.00297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doello S, Burkhardt M, Forchhammer K (2021) The essential role of sodium bioenergetics and ATP homeostasis in the developmental transitions of a cyanobacterium. Curr Biol. https://doi.org/10.1016/j.cub.2021.01.065

  • Drigo B, Kowalchuk GA, Yergeau E, Bezemer TM, Boschker HTS, Van Veen JA (2007) Impact of elevated carbon dioxide on the rhizosphere communities of Carex arenaria and Festuca rubra. Glob Chang Biol 13:2396–2410

    Article  Google Scholar 

  • Dutta H, Dutta A (2016) The microbial aspect of climate change. In: Energy, ecology and environment, vol 1. Joint Center on Global Change and Earth System Science of the University of Maryland and Beijing Normal University, Beijing, pp 209–232

    Google Scholar 

  • Espinosa J, Forchhammer K, Contreras A (2007) Role of the Synechococcus PCC 7942 nitrogen regulator protein PipX in NtcA-controlled processes. Microbiology 153:711–718

    Article  CAS  PubMed  Google Scholar 

  • Fokina O et al (2010) Mechanism of 2-oxoglutarate signaling by the Synechococcus elongatus P II signal transduction protein. Proc Natl Acad Sci U S A 107:19760–19765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forcada-Nadal A, Palomino-Schatzlein M, Neira JL, Pineda-Lucena A, Rubio V (2017) The PipX protein, when not bound to its targets, has its signaling C-terminal Helix in a flexed conformation. Biochemistry 56:3211–3224

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K (2010) Network of PII Signalling protein interactions in unicellular cyanobacteria. Recent Adv Phototrophic Prokaryotes 675:71–90

    Article  CAS  Google Scholar 

  • Forchhammer K, Schwarz R (2019) Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation. Environ Microbiol 21:1173–1184

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K, Selim KA (2020) Carbon/nitrogen homeostasis control in cyanobacteria. FEMS Microbiol Rev 44:33–53

    Article  CAS  PubMed  Google Scholar 

  • Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208

    Article  CAS  PubMed  Google Scholar 

  • García-Domínguez M, Reyes JC, Florencio FJ (1999) Glutamine synthetase inactivation by protein-protein interaction. Proc Natl Acad Sci U S A 96:7161–7166

    Article  PubMed  PubMed Central  Google Scholar 

  • Gionchetta G, Romaní AM, Oliva F, Artigas J (2019) Distinct responses from bacterial, archaeal and fungal streambed communities to severe hydrological disturbances. Sci Rep 9:13506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grandclement C, Tannieres M, Morera S, Dessaux Y, Faure D (2016) Quorum quenching: role in nature and applied. FEMS Microbiol Rev 40:86–116

    Article  CAS  PubMed  Google Scholar 

  • Gründel M et al (2012) Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology (United Kingdom) 158(12):3032–3043. https://doi.org/10.1099/mic.0.062950-0

    Article  CAS  Google Scholar 

  • Hallin S, Bodelier PLE (2020) Grand challenges in terrestrial microbiology: moving on from a decade of progress in microbial biogeochemistry. Front Microbiol 11:981

    Article  PubMed  PubMed Central  Google Scholar 

  • Hauf W et al (2013) Metabolic changes in Synechocystis PCC6803 upon nitrogen-starvation: excess NADPH sustains polyhydroxybutyrate accumulation. Metabolites 3(1):101–118. https://doi.org/10.3390/metabo3010101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huergo LF, Dixon R (2015) The emergence of 2-Oxoglutarate as a master regulator metabolite. Microbiol Mol Biol Rev 79:419–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huergo LF, Chubatsu LS, Souza EM, Pedrosa FO, Steffens MB, Merrick M (2006a) Interactions between PII proteins and the nitrogenase regulatory enzymes DraT and DraG in Azospirillum brasilense. FEBS Lett 580:5232–5236

    Article  CAS  PubMed  Google Scholar 

  • Huergo LF, Souza EM, Araujo MS, Pedrosa FO, Chubatsu LS, Steffens MB, Merrick M (2006b) ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59:326–337

    Article  CAS  PubMed  Google Scholar 

  • Huergo LF, Merrick M, Pedrosa FO, Chubatsu LS, Araujo LM, Souza EM (2007) Ternary complex formation between AmtB, GlnZ and the nitrogenase regulatory enzyme DraG reveals a novel facet of nitrogen regulation in bacteria. Mol Microbiol 66:1523–1535

    CAS  PubMed  Google Scholar 

  • Huergo LF, Merrick M, Monteiro RA, Chubatsu LS, Steffens MB, Pedrosa FO, Souza EM (2009) In vitro interactions between the PII proteins and the nitrogenase regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase (DraT) and dinitrogenase reductase-activating glycohydrolase (DraG) in Azospirillum brasilense. J Biol Chem 284:6674–6682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huergo LF, Chandra G, Merrick M (2013) P(II) signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol Rev 37:251–283

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B Biol Sci 367:1665–1679

    Article  Google Scholar 

  • Jiang P, Ninfa AJ (2009) α-Ketoglutarate controls the ability of the Escherichia coli PII signal transduction protein to regulate the activities of NRII (NtrB) but does not control the binding of PII to NRII. Biochemistry 48:11514–11521

    Article  CAS  PubMed  Google Scholar 

  • Klahn S, Schaal C, Georg J, Baumgartner D, Knippen G, Hagemann M, Muro-Pastor AM, Hess WR (2015) The sRNA NsiR4 is involved in nitrogen assimilation control in cyanobacteria by targeting glutamine synthetase inactivating factor IF7. Proc Natl Acad Sci U S A 112:E6243–E6252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klahn S, Bolay P, Wright PR, Atilho RM, Brewer KI, Hagemann M, Breaker RR, Hess WR (2018) A glutamine riboswitch is a key element for the regulation of glutamine synthetase in cyanobacteria. Nucleic Acids Res 46:10082–10094

    PubMed  PubMed Central  Google Scholar 

  • Klotz A et al (2015) Nitrogen starvation acclimation in Synechococcus elongatus: redox-control and the role of nitrate reduction as an electron sink. Life 5(1):888–904. https://doi.org/10.3390/life5010888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klotz A et al (2016) Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Curr Biol 26(21):2862–2872. https://doi.org/10.1016/j.cub.2016.08.054

    Article  CAS  PubMed  Google Scholar 

  • Koch M et al (2019) PHB is produced from glycogen turn-over during nitrogen starvation in Synechocystis sp. PCC 6803. Int J Mol Sci 20:1942. https://doi.org/10.3390/ijms20081942

    Article  CAS  PubMed Central  Google Scholar 

  • Koch M, Berendzen KW, Forchhammer K (2020) On the role and production of polyhydroxybutyrate (Phb) in the cyanobacterium synechocystis sp. pcc 6803. Life 10. https://doi.org/10.3390/life10040047

  • Loh E, Righetti F, Eichner H, Twittenhoff C, Narberhaus F (2018) RNA thermometers in bacterial pathogens. Microbiol Spectr 6(2). https://doi.org/10.1128/microbiolspec.RWR-0012-2017

  • Kortmann J, Narberhaus F (2012) Bacterial RNA thermometers: molecular zippers and switches. Nat Rev Microbiol 10:255–265

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Nakajima Y, Ishii A, Yamashita M, Yoshida S, Murata M, Kato K, Shiromaru Y, Kato S, Kanasaki Y, Yoshikawa H, Matsutani M, Thanonkeo P, Yamada M (2019) Capacity for survival in global warming: adaptation of mesophiles to the temperature upper limit. PLoS One 14:e0218985

    Article  PubMed  PubMed Central  Google Scholar 

  • Krysenko S, Matthews A, Okoniewski N, Kulik A, Girbas MG, Tsypik O, Meyners CS, Hausch F, Wohlleben W, Bera A (2019) Initial metabolic step of a novel ethanolamine utilization pathway and its regulation in Streptomyces coelicolor M145. mBio 10:e00326-19

    Article  PubMed  PubMed Central  Google Scholar 

  • Lapina T, Selim KA, Forchhammer K, Ermilova E (2018) The PII signaling protein from red algae represents an evolutionary link between cyanobacterial and Chloroplastida PII proteins. Sci Rep 8:790

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Llácer JL et al (2010) Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. Proc Natl Acad Sci U S A 107(35):15397–15402. https://doi.org/10.1073/pnas.1007015107

    Article  PubMed  PubMed Central  Google Scholar 

  • Luque I, Forchhammer K (2008) Nitrogen assimilation and C/N balance sensing, Chapter 13. In: Herrero A, Flores E (eds) The cyanobacteria: molecular biology, genomics and evolution. Caister Academic Press, London

    Google Scholar 

  • Maleki F, Khosravi A, Nasser A, Taghinejad H, Azizian M (2016) Bacterial heat shock protein activity. J Clin Diagn Res 10:BE01–BE03

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merino N, Aronson HS, Bojanova DP, Feyhl-Buska J, Wong ML, Zhang S, Giovannelli D (2019) Living at the extremes: extremophiles and the limits of life in a planetary context. Front Microbiol 10:780

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller DJ, Fort PE (2018) Heat shock proteins regulatory role in neurodevelopment. Front Neurosci 12:821

    Article  PubMed  PubMed Central  Google Scholar 

  • Krysenko S, Okoniewski N, Kulik A, Matthews A, Grimpo J, Wohlleben W, Bera A (2017) Gamma-glutamylpolyamine synthetase GlnA3 is involved in the first step of polyamine degradation pathway in Streptomyces coelicolor M145. Front Microbiol 8:726

    Article  PubMed  PubMed Central  Google Scholar 

  • Muro-Pastor MI, Reyes JC, Florencio FJ (2001) Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276:38320–38328

    Article  CAS  PubMed  Google Scholar 

  • Mus F, Colman DR, Peters JW, Boyd ES (2019) Geobiological feedbacks, oxygen, and the evolution of nitrogenase. Free Radic Biol Med 140:250–259

    Article  CAS  PubMed  Google Scholar 

  • Narberhaus F, Balsiger S (2003) Structure-function studies of Escherichia coli RpoH (σ32) by in vitro linker insertion mutagenesis. J Bacteriol 185:2731–2738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narberhaus F, Waldminghaus T, Chowdhury S (2006) RNA thermometers. FEMS Microbiol Rev 30:3–16

    Article  CAS  PubMed  Google Scholar 

  • Neira JL, Ortore MG, Florencio FJ, Muro-Pastor MI, Rizzuti B (2020) Dynamics of the intrinsically disordered inhibitor IF7 of glutamine synthetase in isolation and in complex with its partner. Arch Biochem Biophys 683:108303

    Article  CAS  PubMed  Google Scholar 

  • Oelze J (2000) Respiratory protection of nitrogenase in azotobacter species: is a widely held hypothesis unequivocally supported by experimental evidence? FEMS Microbiol Rev 24:321–333

    Article  CAS  PubMed  Google Scholar 

  • Orthwein T et al (2020) The novel PII-interacting regulator PirC (Sll0944) identifies 3-phosphoglycerate mutase (PGAM) as central control point of carbon storage metabolism in cyanobacteria. bioRxiv. https://doi.org/10.1101/2020.09.11.292599

  • Pantoja-Uceda D, Neira JL, Saelices L, Robles-Rengel R, Florencio FJ, Muro-Pastor MI, Santoro J (2016) Dissecting the binding between glutamine synthetase and its two natively unfolded protein inhibitors. Biochemistry 55:3370–3382

    Article  CAS  PubMed  Google Scholar 

  • Perez-Mon C, Frey B, Frossard A (2020) Functional and structural responses of arctic and alpine soil prokaryotic and fungal communities under freeze-thaw cycles of different frequencies. Front Microbiol 11:982. https://doi.org/10.3389/fmicb.2020.00982

    Article  PubMed  PubMed Central  Google Scholar 

  • Rajendran C, Gerhardt EC, Bjelic S, Gasperina A, Scarduelli M, Pedrosa FO, Chubatsu LS, Merrick M, Souza EM, Winkler FK, Huergo LF, Li XD (2011) Crystal structure of the GlnZ-DraG complex reveals a different form of PII-target interaction. Proc Natl Acad Sci U S A 108:18972–18976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rampelotto PH (2013) Extremophiles and extreme environments. Life 3:482–485

    Article  PubMed  PubMed Central  Google Scholar 

  • Rexer HU, Schäberle T, Wohlleben W, Engels A (2006) Investigation of the functional properties and regulation of three glutamine synthetase-like genes in Streptomyces coelicolor A3(2). Arch Microbiol 186:447–458

    Article  CAS  PubMed  Google Scholar 

  • Righetti F, Narberhaus F (2014) How to find RNA thermometers. Frontiers in Cellular and Infection. Microbiology 4:132

    Google Scholar 

  • Rodriguez R, Durán P (2020) Natural Holobiome engineering by using native extreme microbiome to counteract the climate change effects. Front Bioeng Biotechnol 8:568

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronneau S, Hallez R (2019) Make and break the alarmone: regulation of (p)ppGpp synthetase/hydrolase enzymes in bacteria. FEMS Microbiol Rev 43:389–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousk J, Bengtson P (2014) Microbial regulation of global biogeochemical cycles. Front Microbiol 5:103. https://doi.org/10.3389/fmicb.2014.00103

    Article  PubMed  PubMed Central  Google Scholar 

  • Rudolph B, Gebendorfer KM, Buchner J, Winter J (2010) Evolution of Escherichia coli for growth at high. J Biol Chem 285:19029–19034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutten PJ, Poole PS (2019) Oxygen regulatory mechanisms of nitrogen fixation in rhizobia. Adv Microb Physiol 75:325–389

    Article  CAS  PubMed  Google Scholar 

  • Sabra W, Zeng AP, Lunsdorf H, Deckwer WD (2000) Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role in protecting nitrogenase. Appl Environ Microbiol 66:4037–4044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saelices L, Galmozzi CV, Florencio FJ, Muro-Pastor MI, Neira JL (2011) The inactivating factor of glutamine synthetase IF17 is an intrinsically disordered protein, which folds upon binding to its target. Biochemistry 50:9767–9778

    Article  CAS  PubMed  Google Scholar 

  • Sandberg TE, Pedersen M, Lacroix RA, Ebrahim A, Bonde M, Herrgard MJ, Palsson BO, Sommer M, Feist AM (2014) Evolution of Escherichia coli to 42 °C and subsequent genetic engineering reveals adaptive mechanisms and novel mutations. Mol Biol Evol 31:2647–2662

    Google Scholar 

  • Sandh G, Xu L, Bergman B (2012) Diazocyte development in the marine diazotrophic cyanobacterium Trichodesmium. Microbiol (Reading) 158:345–352

    Article  CAS  Google Scholar 

  • Sauer J et al (2001) Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. Plant Physiol 126:233–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim KA, Haffner M (2020) Heavy metal stress alters the response of the unicellular cyanobacterium Synechococcus elongatus PCC 7942 to nitrogen starvation. Life (Basel, Switzerland) 10(11):275. https://doi.org/10.3390/life10110275

    Article  CAS  Google Scholar 

  • Selim KA, Maldener I (2021) Cellular and molecular strategies in cyanobacterial survival-“In Memory of Prof. Dr. Wolfgang Lockau”. Life (Basel, Switzerland) 11(2):132. https://doi.org/10.3390/life11020132

    Article  Google Scholar 

  • Selim KA, Haase F, Hartmann MD, Hagemann M, Forchhammer K (2018) PII-like signaling protein SbtB links cAMP sensing with cyanobacterial inorganic carbon response. Proc Natl Acad Sci U S A 115(21):E4861–E4869

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Selim KA, Haffner M, Watzer B, Forchhammer K (2019) Tuning the in vitro sensing and signaling properties of cyanobacterial PII protein by mutation of key residues. Sci Rep 9(1):18985. https://doi.org/10.1038/s41598-019-55495-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim KA, Ermilova E, Forchhammer K (2020c) From cyanobacteria to Archaeplastida: new evolutionary insights into PII signalling in the plant kingdom. New Phytol 227:722–731

    Article  PubMed  Google Scholar 

  • Selim KA, Lapina T, Forchhammer K, Ermilova E (2020b) Interaction of N-acetyl-l-glutamate kinase with the PII signal transducer in the non-photosynthetic alga Polytomella parva: co-evolution towards a hetero-oligomeric enzyme. FEBS J 287:465–482

    Article  CAS  PubMed  Google Scholar 

  • Selim KA, Tremiño L, Alva V, Espinosa J, Contreras A, Marco-Marín C, Hartmann MD, Forchhammer K, Rubio V (2020a) Functional and structural characterization of PII-like protein CutA does not support involvement in heavy metal tolerance in cyanobacteria and hints at a small-molecule carrying/signaling role. FEBS J. https://doi.org/10.1111/febs.15464

  • Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JBH, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi Y, Zhao W, Zhang W, Ye Z, Zhao J (2006) Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 103:11334–11339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790

    Article  CAS  PubMed  Google Scholar 

  • Smith TP, Thomas T, García-Carreras B, Sal S, Yvon-Durocher G, Bell T, Pawar S (2019) Community-level respiration of prokaryotic microbes may rise with global warming. Nat Commun 10(1):5124. https://doi.org/10.1038/s41467-019-13109-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spät P et al (2018) Chlorosis as a developmental program in cyanobacteria: the proteomic fundament for survival and awakening. Mol Cell Proteomics 17:1650–1669

    Article  PubMed  PubMed Central  Google Scholar 

  • Steinchen W, Bange G (2016) The magic dance of the alarmones (p)ppGpp. Mol Microbiol 101:531–544

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Thakur R, Shankar J (2015) Role of heat-shock proteins in cellular function and in the biology of fungi. Biotechnol Res Int 132635

    Google Scholar 

  • Voolstra CR, Ziegler M (2020) Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. BioEssays 42(7):e2000004

    Article  PubMed  Google Scholar 

  • Walter J, Lynch F, Battchikova N, Aro EM, Gollan PJ (2016) Calcium impacts carbon and nitrogen balance in the filamentous cyanobacterium Anabaena sp. PCC 7120. J Exp Bot 67:3997–4008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walter J, Selim KA, Leganés F, Fernández-Piñas F, Vothknecht UC, Forchhammer K, Aro EM, Gollan PJ (2019) A novel Ca2+-binding protein influences photosynthetic electron transport in Anabaena sp. PCC 7120. Biochim Biophys Acta Bioenerg 1860:519–532

    Article  CAS  PubMed  Google Scholar 

  • Walter J, Leganés F, Aro EM, Gollan PJ (2020) The small Ca2+-binding protein CSE links Ca2+ signalling with nitrogen metabolism and filament integrity in Anabaena sp. PCC 7120. BMC Microbiol 20(1):57. https://doi.org/10.1186/s12866-020-01735-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, DeHaseth PL (2003) Sigma 32-dependent promoter activity in vivo: sequence determinants of the groE promoter. J Bacteriol 185:5800–5806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wooliver R, Tittes SB, Sheth SN (2020) A resurrection study reveals limited evolution of thermal performance in response to recent climate change across the geographic range of the scarlet monkeyflower. Evolution. https://doi.org/10.1111/evo.1404

  • Xue K, Xie J, Zhou A, Liu F, Li D, Wu L, Deng Y, He Z, Van Nostrand JD, Luo Y, Zhou J (2016) Warming alters expressions of microbial functional genes important to ecosystem functioning. Front Microbiol 7:668. https://doi.org/10.3389/fmicb.2016.00668

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Yang S, Van Nostrand JD, Zhou J, Fang W, Qi Q, Liu Y, Wullschleger SD, Liang L, Graham DE, Yang Y, Gu B (2017) Microbial community and functional gene changes in Arctic Tundra soils in a microcosm warming experiment. Front Microbiol 8:1741. https://doi.org/10.3389/fmicb.2017.01741

    Article  PubMed  PubMed Central  Google Scholar 

  • Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. Trends Ecol Evol 21:288–295

    Article  PubMed  Google Scholar 

  • Zhao Y, Shi Y, Zhao W, Huang X, Wang D, Brown N, Brand J, Zhao J (2005) CcbP, a calcium-binding protein from Anabaena sp. PCC 7120, provides evidence that calcium ions regulate heterocyst differentiation. Proc Natl Acad Sci U S A 102:5744–5448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zilliges Y (2014) Glycogen, a dynamic cellular sink and reservoir for carbon. In: Flores E (ed) Cell biology. Caister Academic Press, London

    Google Scholar 

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Acknowledgments

The authors gratefully acknowledge Karl Forchhammer for continued support. Furthermore, we would like to acknowledge Libera Lo-Presti for critical scientific and linguistic editing of the manuscript and the infrastructural support by the Cluster of Excellence “Controlling Microbes to Fight Infections” (EXC 2124) of the German research foundation (DFG). We are indebted to the DFG for continuous funding of the work in the authors laboratory. KAS would like to dedicate this chapter to the memory of Dr. Ali Selim, a distinguished father and medical doctor, for his continued support.

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Authors and Affiliations

  1. Organismic Interactions Department, Interfaculty Institute for Microbiology and Infection Medicine, Cluster of Excellence ‘Controlling Microbes to Fight Infections’, Tübingen University, Tübingen, Germany

    Khaled A. Selim, Erik Zimmer & Sofía Doello

  2. Chemistry of Natural and Microbial Products Department, Pharmaceutical and Drug Industries Research Division, National Research Centre, Cairo, Egypt

    Khaled A. Selim & Heba Yehia

Authors
  1. Khaled A. Selim
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  2. Erik Zimmer
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  3. Heba Yehia
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  4. Sofía Doello
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Corresponding author

Correspondence to Khaled A. Selim .

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Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    D. K. Choudhary

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Arti Mishra

  3. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

Ethics declarations

KAS conceived and designed this project. All authors analyzed the data and wrote the manuscript, while KSA merged the final version of the manuscript. KAS and EZ prepared the figures (except Fig. 36.8 by SD). All authors but particularly SD commented and edited on the manuscript and approved the final version of the manuscript.

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Selim, K.A., Zimmer, E., Yehia, H., Doello, S. (2021). Molecular and Cellular Mechanisms Underlying the Microbial Survival Strategies: Insights into Temperature and Nitrogen Adaptations. In: Choudhary, D.K., Mishra, A., Varma, A. (eds) Climate Change and the Microbiome. Soil Biology, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-030-76863-8_36

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