Advertisement

Cyclic di-GMP Signaling in Extreme Acidophilic Bacteria

  • Matías CastroEmail author
  • Mauricio Díaz
  • Ana Moya Beltrán
  • Nicolas GuilianiEmail author
Chapter
  • 109 Downloads

Abstract

Extreme acidophilic bacteria are a phylogenetically diverse group of microorganisms that grow optimally at pH values below 3. They thrive in natural or man-made environments where life is challenged by extreme acidity, low availability of organic matter, and high concentrations of heavy metals. Most acidophilic bacteria are chemolitho(auto)trophs, obtaining energy from the oxidation of metal sulfides, one of the most abundant mineral classes on earth. Bacterial attachment on mineral surface and the subsequent biofilm development plays critical role in mineral dissolution, which is directly related with ecologic phenomena and biotechnological applications, such as acid mine drainage, biogeochemical cycles, and bioleaching processes. In contrast to well-studied neutrophilic bacterial strains, the understanding of cyclic di-GMP signaling in extreme acidophilic bacteria is still incipient. However, significant progress has been made in the last several years through global genomic analysis on acidophilic communities, and genetic work on species belonging to the most iconic acidophilic genus, Acidithiobacillus. This chapter presents an overview of molecular insights into cyclic di-GMP signaling obtained from At. ferrooxidans, At. caldus, and At. thioooxidans. In addition, it describes the cyclic di-GMP signaling network as a widespread but highly diverse mechanism used by acidophilic bacteria to transduce environmental signals into biofilm-related responses mainly driven by cyclic di-GMP effector proteins involved in swarming motility and the production of exopolymeric substances.

Keywords

Acidithiobacillus Acidophilic bacteria Biofilm Cyclic di-GMP pathway Extremophile 

References

  1. 1.
    Johnson DB, Quatrini R (2016) Acidophile microbiology in space and time. In: Quatrini R, Johnson DB (eds) Acidophiles: life in extremely acidic environments. Caister Academic Press, London, pp 1–16.  https://doi.org/10.21775/9781910190333.16 Google Scholar
  2. 2.
    Garcia-Moyano A, González-Toril E, Aguilera A, Amils R (2007) Prokaryotic community composition and ecology of floating macroscopic filaments from an extreme acidic environment, Río Tinto (SW, Spain). Syst Appl Microbiol 30:601–614CrossRefGoogle Scholar
  3. 3.
    Nancucheo I, Johnson DB (2010) Production of glycolic acid by chemolithotrophic iron- and sulfur-oxidizing bacteria and its role in delineating and sustaining acidophilic sulfide mineral-oxidizing consortia. Appl Environ Microbiol 76:461–467CrossRefGoogle Scholar
  4. 4.
    Moya-Beltrán A, Rojas C, Díaz M, Guiliani N, Quatrini R, Castro M (2019) Nucleotide second messenger-based signaling in extreme acidophiles of the Acidithiobacillus species complex: partition between the core and variable gene complements. Front Microbiol 10:381.  https://doi.org/10.3389/fmicb.2019.00381 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K (2015) Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13(5):298–309.  https://doi.org/10.1038/nrmicro3448 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    McDonough KA, Rodriguez A (2011) The myriad roles of cyclic AMP in microbial pathogens: from signal to sword. Nat Rev Microbiol 10(1):27–38.  https://doi.org/10.1038/nrmicro2688 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1–52.  https://doi.org/10.1128/MMBR.00043-12 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Corrigan RM, Gründling A (2013) Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 11(8):513–524.  https://doi.org/10.1038/nrmicro3069 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Sinha SC, Sprang SR (2006) Structures, mechanism, regulation and evolution of class III nucleotidyl cyclases. Rev Physiol Biochem Pharmacol 157:105–140CrossRefGoogle Scholar
  10. 10.
    Atkinson GC, Tenson T, Hauryliuk V (2011) The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life. PLoS One 6(8):e23479.  https://doi.org/10.1371/journal.pone.0023479 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sismeiro O, Trotot P, Biville F, Vivares C, Danchin A (1998) Aeromonas hydrophila adenylyl cyclase 2: a new class of adenylyl cyclases with thermophilic properties and sequence similarities to proteins from hyperthermophilic archaebacteria. J Bacteriol 180(13):3339–3344CrossRefGoogle Scholar
  12. 12.
    Smith N, Kim SK, Reddy PT, Gallagher DT (2006) Crystallization of the class IV adenylyl cyclase from Yersinia pestis. Acta Crystallogr Sect F Struct Biol Cryst Commun 62(Pt 3):200–204CrossRefGoogle Scholar
  13. 13.
    Tumlirsch T, Jendrossek D (2017) Proteins with CHADs (conserved Histidine α-helical domains) are attached to polyphosphate granules in vivo and constitute a novel family of polyphosphate-associated proteins (Phosins). Appl Environ Microbiol 83(7):e03399–e03316.  https://doi.org/10.1128/AEM.03399-16 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Navarro C, von Bernath D, Jerez CA (2013) Heavy metal resistance strategies of acidophilic bacteria and their acquisition: importance for biomining and bioremediation. Biol Res 46:363–371CrossRefGoogle Scholar
  15. 15.
    Anantharaman V, Aravind L (2001) The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci 26(10):579–582CrossRefGoogle Scholar
  16. 16.
    Gavira JA, Ortega Á, Martín-Mora D, Conejero-Muriel MT, Corral-Lugo A, Morel B, Matilla MA, Krell T (2018) Structural basis for polyamine binding at the dCACHE domain of the McpU chemoreceptor from pseudomonas putida. J Mol Biol 430(13):1950–1963.  https://doi.org/10.1016/j.jmb.2018.05.008 CrossRefPubMedGoogle Scholar
  17. 17.
    Finkbeiner M, Grischin J, Seth A, Schultz JE (2019) In search of a function for the membrane anchors of class IIIa adenylate cyclases. Int J Med Microbiol S1438-4221(19):30021–30029.  https://doi.org/10.1016/j.ijmm.2019.03.006 CrossRefGoogle Scholar
  18. 18.
    Green J, Stapleton MR, Smith LJ, Artymiuk PJ, Kahramanoglou C, Hunt DM, Buxton RS (2014) Cyclic-AMP and bacterial cyclic-AMP receptor proteins revisited: adaptation for different ecological niches. Curr Opin Microbiol 18:1–7.  https://doi.org/10.1016/j.mib.2014.01.003 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Witte G, Hartung S, Büttner K, Hopfner KP (2008) Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell 30(2):167–178.  https://doi.org/10.1016/j.molcel.2008.02.020 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Winther KS, Roghanian M, Gerdes K (2018) Activation of the stringent response by loading of RelA-tRNA complexes at the ribosomal A-site. Mol Cell 70(1):95–105.e4.  https://doi.org/10.1016/j.molcel.2018.02.033 CrossRefPubMedGoogle Scholar
  21. 21.
    Battesti A, Bouveret E (2009) Bacteria possessing two RelA/SpoT-like proteins have evolved a specific stringent response involving the acyl carrier protein-SpoT interaction. J Bacteriol 191(2):616–624.  https://doi.org/10.1128/JB.01195-08 CrossRefPubMedGoogle Scholar
  22. 22.
    da Costa Vasconcelos FN, Maciel NK, Favaro DC, de Oliveira LC, Barbosa AS, Salinas RK et al (2017) Structural and enzymatic characterization of a cAMP-dependent diguanylate cyclase from pathogenic Leptospira species. J Mol Biol 429(15):2337–2352.  https://doi.org/10.1016/j.jmb.2017.06.002 CrossRefPubMedGoogle Scholar
  23. 23.
    Chen HJ, Li N, Luo Y, Jiang YL, Zhou CZ, Chen Y et al (2018) The GDP-switched GAF domain of DcpA modulates the concerted synthesis/hydrolysis of c-di-GMP in Mycobacterium smegmatis. Biochem J 475(7):1295–1308.  https://doi.org/10.1042/BCJ20180079 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Qi Y, Rao F, Luo Z, Liang ZX (2009) A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 48(43):10275–10285.  https://doi.org/10.1021/bi901121w CrossRefPubMedGoogle Scholar
  25. 25.
    Chang AL, Tuckerman JR, Gonzalez G, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M, Gilles-Gonzalez MA (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40(12):3420–3426CrossRefGoogle Scholar
  26. 26.
    Tuckerman JR, Gonzalez G, Sousa EH, Wan X, Saito JA, Alam M, Gilles-Gonzalez MA (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48(41):9764–9774.  https://doi.org/10.1021/bi901409g CrossRefPubMedGoogle Scholar
  27. 27.
    Rawlings DE (2005) Characteristics and adaptability of iron- and sulfur-oxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb Cell Factor 4:13.  https://doi.org/10.1186/1475-2859-4-13 CrossRefGoogle Scholar
  28. 28.
    Zschiedrich CP, Keidel V, Szurmant H (2016) Molecular mechanisms of two- component signal transduction. J Mol Biol 428:3752–3775CrossRefGoogle Scholar
  29. 29.
    Guzzo CR, Salinas RK, Andrade MO, Farah CS (2009) PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 393(4):848–866.  https://doi.org/10.1016/j.jmb.2009.07.065 CrossRefGoogle Scholar
  30. 30.
    O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30(2):295–304CrossRefGoogle Scholar
  31. 31.
    Semmler AB, Whitchurch CB, Mattick JS (1999) A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145(10):2863–2873CrossRefGoogle Scholar
  32. 32.
    Ryjenkov DA, Simm R, Römling U, Gomelsky M (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281(41):30310–30314CrossRefGoogle Scholar
  33. 33.
    Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S (2007) The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65(4):876–895CrossRefGoogle Scholar
  34. 34.
    Morgan JL, McNamara JT, Zimmer J (2014 May) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol 21(5):489–496.  https://doi.org/10.1038/nsmb.2803 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Francke C, Groot Kormelink T, Hagemeijer Y, Overmars L, Sluijter V, Moezelaar R, Siezen RJ (2011) Comparative analyses imply that the enigmatic sigma factor 54 is a central controller of the bacterial exterior. BMC Genomics 12(1):385.  https://doi.org/10.1186/1471-2164-12-385 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Hallberg K, González-Toril E, Johnson D (2010) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19.  https://doi.org/10.1007/s00792-009-0282-y CrossRefPubMedGoogle Scholar
  37. 37.
    Hallberg KB, Lindström EB (1994) Characterization of Thiobacillus caldus sp. nov., a moderately thermophilic acidophile. Microbiology 140(12):3451–3456CrossRefGoogle Scholar
  38. 38.
    Castro M, Moya-Beltrán A, Covarrubias PC, Gonzalez M, Cardenas JP, Issotta F, Nuñez H, Acuña LG, Encina G, Holmes DS, Johnson DB, Quatrini R (2017) Draft genome sequence of the type strain of the sulfur-oxidizing acidophile, Acidithiobacillus albertensis (DSM 14366). Stand Genomic Sci 12:77.  https://doi.org/10.1186/s40793-017-0282-y CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Valdés J, Pedroso I, Quatrini R, Holmes DS (2008) Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: insights into their metabolism and ecophysiology. Hydrometallurgy 94:180–184CrossRefGoogle Scholar
  40. 40.
    Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and súlfur. Appl Environ Microbiol 65(1):319–321CrossRefGoogle Scholar
  41. 41.
    Vera M, Schippers A, Sand W (2013) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation--part A. Appl Microbiol Biotechnol 97(17):7529–7541.  https://doi.org/10.1007/s00253-013-4954-2 CrossRefPubMedGoogle Scholar
  42. 42.
    Ruiz LM, Castro M, Barriga A, Jerez CA, Guiliani N (2012) The extremophile Acidithiobacillus ferrooxidans possesses a c-di-GMP signalling pathway that could play a significant role during bioleaching of minerals. Lett Appl Microbiol 54:133–139CrossRefGoogle Scholar
  43. 43.
    Diaz M, Copaja S, Guiliani N (2013) Functional analysis of c-di-GMP pathway in biomining bacteria Acidithiobacillus thiooxidans. Adv Mater Res 825:133–136CrossRefGoogle Scholar
  44. 44.
    Díaz M, Castro M, Copaja S, Guiliani N (2018) Biofilm formation by the Acidophile bacterium Acidithiobacillus thiooxidans involves c-di-GMP pathway and Pel exopolysaccharide. Genes (Basel) 9(2):E113.  https://doi.org/10.3390/genes9020113 CrossRefGoogle Scholar
  45. 45.
    Castro M, Ruíz LM, Barriga A, Jerez CA, Holmes DS, Guiliani N (2009) C-di-GMP pathway in biomining bacteria. Adv Mater Res 71–73:223–226.  https://doi.org/10.4028/www.scientific.net/AMR.71-73.223 CrossRefGoogle Scholar
  46. 46.
    Castro M, Deane S, Ruiz L, Rawlings DE, Guiliani N (2015) Diguanylate Cyclase null mutant reveals that C-Di-GMP pathway regulates the motility and adherence of the extremophile bacterium Acidithiobacillus caldus. PLoS One 10(2):e0116399.  https://doi.org/10.1371/journal.pone.0116399 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Ryan RP, Tolker-Nielsen T, Dow JM (2012) When the PilZ don’t work: effectors for cyclic di-GMP action in bacteria. Trends Microbiol 20(5):235–242CrossRefGoogle Scholar
  48. 48.
    Friedman F, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51(3):675–690CrossRefGoogle Scholar
  49. 49.
    Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65(6):1474–1484CrossRefGoogle Scholar
  50. 50.
    Zähringer F, Lacanna E, Jenal U, Schirmer T, Boehm A (2013) Structure and signaling mechanism of a zinc-sensory diguanylate cyclase. Structure 21(7):1149–1157.  https://doi.org/10.1016/j.str.2013.04.026 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Fundación Ciencia y VidaSantiagoChile
  2. 2.Millennium Nucleus in the Biology of Intestinal MicrobiotaSantiagoChile
  3. 3.Facultad de Ingeniería y TecnologíaUniversidad San SebastianConcepciónChile
  4. 4.Department of Biology, Faculty of SciencesUniversidad de ChileSantiagoChile

Personalised recommendations