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Cyclic di-AMP in Bacillus subtilis Biofilm Formation

  • Sarah M. Yannarell
  • Loni Townsley
  • Elizabeth A. ShankEmail author
Chapter

Abstract

Bacillus subtilis is a soil-dwelling bacterium that forms highly structured microbial communities called biofilms. Biofilm formation is important for bacterial survival, as biofilms are highly tolerant to environmental stresses. In B. subtilis, the formation of biofilms facilitates important interactions with plants. While the genetic regulation of biofilm formation is highly studied in B. subtilis, little is known regarding the molecular details of how signaling molecules feed into the biofilm regulatory network of this bacterium. Recent studies found that the second messenger cyclic di-adenylate monophosphate (cyclic di-AMP) plays an important role in B. subtilis biofilm formation and plant attachment. B. subtilis secretes cyclic di-AMP via three putative cyclic di-AMP transporters, suggesting that cyclic di-AMP can act as an extracellular signal for biofilm formation and plant attachment. Here, we discuss how cyclic di-AMP metabolism and secretion impact colony biofilm architecture, biofilm gene expression, and plant attachment in B. subtilis and speculate on future directions for the field.

Keywords

Bacillus subtilis Cyclic di-AMP Cyclic dinucleotide signaling Second messengers Biofilms 

References

  1. 1.
    Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108.  https://doi.org/10.1038/nrmicro821 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575.  https://doi.org/10.1038/nrmicro.2016.94 CrossRefPubMedGoogle Scholar
  3. 3.
    Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633.  https://doi.org/10.1038/nrmicro2415 CrossRefPubMedGoogle Scholar
  4. 4.
    Hobley L, Harkins C, Macphee CE, Stanley-Wall NR (2015) Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol Rev 39:649–669.  https://doi.org/10.1093/femsre/fuv015 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Dragoš A, Kovács ÁT (2017) The peculiar functions of the bacterial extracellular matrix. Trends Microbiol 25:257–266.  https://doi.org/10.1016/j.tim.2016.12.010 CrossRefPubMedGoogle Scholar
  6. 6.
    Nadell CD, Drescher K, Wingreen NS, Bassler BL (2015) Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9:1700–1709.  https://doi.org/10.1038/ismej.2014.246 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210.  https://doi.org/10.1038/nrmicro1838 CrossRefPubMedGoogle Scholar
  8. 8.
    van Gestel J, Vlamakis H, Kolter R (2015) From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol e1002141:13.  https://doi.org/10.1371/journal.pbio.1002141 CrossRefGoogle Scholar
  9. 9.
    Claessen D, Rozen DE, Kuipers OP, Søgaard-Andersen L, van Wezel GP (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12:115–124.  https://doi.org/10.1038/nrmicro3178 CrossRefPubMedGoogle Scholar
  10. 10.
    Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91.  https://doi.org/10.1016/j.tim.2013.12.004 CrossRefPubMedGoogle Scholar
  11. 11.
    Yan J, Nadell CD, Bassler BL (2017) Environmental fluctuation governs selection for plasticity in biofilm production. ISME J 11:1569–1577.  https://doi.org/10.1038/ismej.2017.33 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168.  https://doi.org/10.1038/nrmicro2960 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238.  https://doi.org/10.1111/j.1365-2958.2005.05020.x CrossRefPubMedGoogle Scholar
  14. 14.
    Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci 107:2230–2234.  https://doi.org/10.1073/pnas.0910560107 CrossRefPubMedGoogle Scholar
  15. 15.
    Kobayashi K, Iwano M (2012) BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85:51–66.  https://doi.org/10.1111/j.1365-2958.2012.08094.x CrossRefPubMedGoogle Scholar
  16. 16.
    Gonzalez-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science 301:510–513.  https://doi.org/10.1126/science.1086462 CrossRefPubMedGoogle Scholar
  17. 17.
    Piggot PJ, Hilbert DW (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7:579–586.  https://doi.org/10.1016/j.mib.2004.10.001 CrossRefPubMedGoogle Scholar
  18. 18.
    Kearns DB, Losick R (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19:3083–3094.  https://doi.org/10.1101/gad.1373905 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Vlamakis H, Aguilar C, Losick R, Kolter R (2008) Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945–953.  https://doi.org/10.1101/gad.1645008 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Dragoš A, Kiesewalter H, Martin M, Hsu CY, Hartmann R, Wechsler T, Eriksen C, Brix S, Drescher K, Stanley-Wall N, Kümmerli R, Kovács ÁT (2018) Division of labor during biofilm matrix production. Curr Biol 28:1903–1913.  https://doi.org/10.1016/j.cub.2018.04.046 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Lopez D, Vlamakis H, Kolter R (2009) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33:152–163.  https://doi.org/10.1111/j.1574-6976.2008.00148.x CrossRefPubMedGoogle Scholar
  22. 22.
    López D, Vlamakis H, Losick R, Kolter R (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618.  https://doi.org/10.1111/j.1365-2958.2009.06882.x CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Ackermann M (2015) A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol 13:497–508.  https://doi.org/10.1038/nrmicro3491 CrossRefPubMedGoogle Scholar
  24. 24.
    Davis KM, Isberg RR (2016) Defining heterogeneity within bacterial populations via single cell approaches. BioEssays 38:782–790.  https://doi.org/10.1002/bies.201500121 CrossRefPubMedGoogle Scholar
  25. 25.
    Aguilar C, Vlamakis H, Guzman A, Losick R, Kolter R (2010) KinD is a checkpoint protein linking spore formation to extracellular-matrix production in Bacillus subtilis biofilms. MBio 1:e00035–e00010.  https://doi.org/10.1128/mBio.00035-10 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42:1199–1209CrossRefGoogle Scholar
  27. 27.
    Molle V, Fujita M, Jensen ST, Eichenberger P, González-Pastor JE, Liu JS, Losick R (2003) The Spo0A regulon of Bacillus subtilis. Mol Microbiol 50:1683–1701.  https://doi.org/10.1046/j.1365-2958.2003.03818.x CrossRefPubMedGoogle Scholar
  28. 28.
    Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187:1357–1368.  https://doi.org/10.1128/JB.187.4.1357-1368.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Jiang M, Shao W, Perego M, Hoch JA (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38:535–542.  https://doi.org/10.1046/j.1365-2958.2000.02148.x CrossRefPubMedGoogle Scholar
  30. 30.
    Ireton K, Rudner DZ, Siranosian KJ, Grossman AD (1993) Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev 7:283–294CrossRefGoogle Scholar
  31. 31.
    McLoon AL, Kolodkin-Gal I, Rubinstein SM, Kolter R, Losick R (2011) Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J Bacteriol 193:679–685.  https://doi.org/10.1128/JB.01186-10 CrossRefPubMedGoogle Scholar
  32. 32.
    López D, Fischbach M, Chu F, Losick R, Kolter R (2009) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci 106:280–285.  https://doi.org/10.1073/pnas.0810940106 CrossRefPubMedGoogle Scholar
  33. 33.
    Shemesh M, Kolter R, Losick R (2010) The biocide chlorine dioxide stimulates biofilm formation in Bacillus subtilis by activation of the histidine kinase KinC. J Bacteriol 192:6352–6356.  https://doi.org/10.1128/JB.01025-10 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci 110:E1621–E1630.  https://doi.org/10.1073/pnas.1218984110 CrossRefPubMedGoogle Scholar
  35. 35.
    Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo JH, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430.  https://doi.org/10.1111/j.1365-2958.2012.08109.x CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Corrigan RM, Gründling A (2013) Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 11:513–524.  https://doi.org/10.1038/nrmicro3069 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    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 30:167–178.  https://doi.org/10.1016/j.molcel.2008.02.020 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Rosenberg J, Dickmanns A, Neumann P, Gunka K, Arens J, Kaever V, Stülke J, Ficner R, Commichau FM (2015) Structural and biochemical analysis of the essential diadenylate cyclase CdaA from Listeria monocytogenes. J Biol Chem 290:6596–6606.  https://doi.org/10.1074/jbc.M114.630418 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Römling U (2008) Great times for small molecules: c-di-AMP, a second messenger candidate in bacteria and archaea. Sci Signal 1:pe39.  https://doi.org/10.1126/scisignal.133pe39 CrossRefPubMedGoogle Scholar
  40. 40.
    Mehne FMP, Gunka K, Eilers H, Herzberg C, Kaever V, Stülke J (2013) Cyclic di-AMP homeostasis in Bacillus subtilis: both lack and high level accumulation of the nucleotide are detrimental for cell growth. J Biol Chem 288:2004–2017.  https://doi.org/10.1074/jbc.M112.395491 CrossRefPubMedGoogle Scholar
  41. 41.
    Tan E, Rao F, Pasunooti S, Pham TH, Soehano I, Turner MS, Liew CW, Lescar J, Pervushin K, Liang ZX (2013) Solution structure of the PAS domain of a thermophilic YybT protein homolog reveals a potential ligand-binding site. J Biol Chem 288:11949–11959.  https://doi.org/10.1074/jbc.M112.437764 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Rao F, See RY, Zhang D, Toh DC, Ji Q, Liang ZX (2010) YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J Biol Chem 285:473–482.  https://doi.org/10.1074/jbc.M109.040238 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Huynh TN, Luo S, Pensinger D, Sauer JD, Tong L, Woodward JJ (2015) An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc Natl Acad Sci 112:E747–E756.  https://doi.org/10.1073/pnas.1416485112 CrossRefPubMedGoogle Scholar
  44. 44.
    Huynh TN, Woodward JJ (2016) Too much of a good thing: regulated depletion of c-di-AMP in the bacterial cytoplasm. Curr Opin Microbiol 30:22–29.  https://doi.org/10.1016/j.mib.2015.12.007 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Commichau FM, Dickmanns A, Gundlach J, Ficner R, Stülke J (2015) A jack of all trades: the multiple roles of the unique essential second messenger cyclic di-AMP. Mol Microbiol 97:189–204.  https://doi.org/10.1111/mmi.13026 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Commichau FM, Gibhardt J, Halbedel S, Gundlach J, Stülke J (2018) A Delicate connection: c-di-AMP affects cell integrity by controlling osmolyte transport. Trends Microbiol 26:175–185.  https://doi.org/10.1016/j.tim.2017.09.003 CrossRefPubMedGoogle Scholar
  47. 47.
    Luo Y, Helmann JD (2012) Analysis of the role of Bacillus subtilis σM in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 83:623–639.  https://doi.org/10.1111/j.1365-2958.2011.07953.x CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Gundlach J, Mehne FMP, Herzberg C, Kampf J, Valerius O, Kaever V, Stülke J (2015) An essential poison: synthesis and degradation of cyclic di-AMP in Bacillus subtilis. J Bacteriol 197:3265–3274.  https://doi.org/10.1128/JB.00564-15 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Townsley L, Yannarell SM, Huynh TN, Woodward JJ, Shank EA (2018) Cyclic di-AMP acts as an extracellular signal that impacts Bacillus subtilis biofilm formation and plant attachment. MBio 9:e00341–e00318.  https://doi.org/10.1128/mBio.00341-18 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Du B, Ji W, An H, Shi Y, Huang Q, Cheng Y, Fu Q, Wang H, Yan Y, Sun J (2014) Functional analysis of c-di-AMP phosphodiesterase, GdpP, in Streptococcus suis serotype 2. Microbiol Res 169:749–758.  https://doi.org/10.1016/j.micres.2014.01.002 CrossRefPubMedGoogle Scholar
  51. 51.
    Konno H, Yoshida Y, Nagano K, Takebe J, Hasegawa Y (2018) Biological and biochemical roles of two distinct cyclic dimeric adenosine 3′,5′-monophosphate- associated phosphodiesterases in Streptococcus mutans. Front Microbiol 9:2347.  https://doi.org/10.3389/fmicb.2018.02347 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Gundlach J, Rath H, Herzberg C, Mäder U, Stülke J (2016) Second messenger signaling in Bacillus subtilis: accumulation of cyclic di-AMP inhibits biofilm formation. Front Microbiol 7:804.  https://doi.org/10.3389/fmicb.2016.00804 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Gundlach J, Commichau FM, Stülke J (2018) Perspective of ions and messengers: an intricate link between potassium, glutamate, and cyclic di-AMP. Curr Genet 64:191–195.  https://doi.org/10.1007/s00294-017-0734-3 CrossRefGoogle Scholar
  54. 54.
    Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Süel GM (2015) Ion channels enable electrical communication in bacterial communities. Nature 527:59–63.  https://doi.org/10.1038/nature15709 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Jones CP, Ferre-D’Amare AR (2014) Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J 33:2692–2703.  https://doi.org/10.15252/embj.201489209 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Meehan RE, Torgerson CD, Gaffney BL, Jones RA, Strobel SA (2016) Nuclease-resistant c-di-AMP derivatives that differentially recognize RNA and protein receptors. Biochemistry 55:837–849.  https://doi.org/10.1021/acs.biochem.5b00965 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kim H, Youn S-J, Kim SO, Ko J, Lee J-O, Choi B-S (2015) Structural studies of potassium transport protein KtrA regulator of conductance of K + (RCK) C domain in complex with cyclic diadenosine monophosphate (c-di-AMP). J Biol Chem 290:16393–16402.  https://doi.org/10.1074/jbc.M115.641340 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Gundlach J, Herzberg C, Kaever V, Gunka K, Hoffmann T, Weiß M, Gibhardt J, Thürmer A, Hertel D, Daniel R, Bremer E, Commichau FM, Stülke J (2017) Control of potassium homeostasis is an essential function of the second messenger cyclic di-AMP in Bacillus subtilis. Sci Signal 10:eaal3011.  https://doi.org/10.1126/scisignal.aal3011 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Holtmann G, Bakker EP, Uozumi N, Bremer E (2003) KtrAB and KtrCD: two K+ uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J Bacteriol 185:1289–1298.  https://doi.org/10.1128/JB.185.4.1289-1298.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR (2013) Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol 9:834–839.  https://doi.org/10.1038/nchembio.1363 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Gründling A (2013) Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc Natl Acad Sci 110:9084–9089.  https://doi.org/10.1073/pnas.1300595110 CrossRefPubMedGoogle Scholar
  62. 62.
    Watson PY, Fedor MJ (2012) The ydaO motif is an ATP-sensing riboswitch in Bacillus subtilis. Nat Chem Biol 8:963–965.  https://doi.org/10.1038/nchembio.1095 CrossRefGoogle Scholar
  63. 63.
    Ren A, Patel DJ (2014) c-di-AMP binds the ydaO riboswitch in two pseudo-symmetry–related pockets. Nat Chem Biol 10:780–786.  https://doi.org/10.1038/nchembio.1606 CrossRefGoogle Scholar
  64. 64.
    Gundlach J, Dickmanns A, Schröder-Tittmann K, Neumann P, Kaesler J, Kampf J, Herzberg C, Hammer E, Schwede F, Kaever V, Tittmann K, Stülke J, Ficner R (2015) Identification, characterization, and structure analysis of the cyclic di-AMP-binding PII-like signal transduction protein DarA. J Biol Chem 290:3069–3080.  https://doi.org/10.1074/jbc.M114.619619 CrossRefGoogle Scholar
  65. 65.
    Block KF, Hammond MC, Breaker RR (2010) Evidence for widespread gene control function by the ydaO riboswitch candidate. J Bacteriol 192:3983–3989.  https://doi.org/10.1128/JB.00450-10 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Oppenheimer-Shaanan Y, Wexselblatt E, Katzhendler J, Yavin E, Ben-Yehuda S (2011) c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep 12:594–601.  https://doi.org/10.1038/embor.2011.77 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Bejerano-Sagie M, Oppenheimer-Shaanan Y, Berlatzky I, Rouvinski A, Meyerovich M, Ben-Yehuda S (2006) A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 125:679–690.  https://doi.org/10.1016/j.cell.2006.03.039 CrossRefPubMedGoogle Scholar
  68. 68.
    Gándara C, de DKC L, Torres R, Serrano E, Altenburger S, Graumann PL, Alonso JC (2017) Activity and in vivo dynamics of Bacillus subtilis DisA are affected by RadA/Sms and by Holliday junction-processing proteins. DNA Repair (Amst) 55:17–30.  https://doi.org/10.1016/j.dnarep.2017.05.002 CrossRefGoogle Scholar
  69. 69.
    Campos SS, Ibarra-Rodriguez JR, Barajas-Ornelas RC, Ramirez-Guadiana FH, Obregon-Herrera A, Setlow P, Pedraza-Reyes M (2014) Interaction of apurinic/apyrimidinic endonucleases Nfo and ExoA with the DNA integrity scanning protein DisA in the processing of oxidative DNA damage during Bacillus subtilis spore outgrowth. J Bacteriol 196:568–578.  https://doi.org/10.1128/JB.01259-13 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Raguse M, Torres R, Seco EM, Gándara C, Ayora S, Moeller R, Alonso JC (2017) Bacillus subtilis DisA helps to circumvent replicative stress during spore revival. DNA Repair (Amst) 59:57–68.  https://doi.org/10.1016/J.DNAREP.2017.09.006 CrossRefGoogle Scholar
  71. 71.
    Gándara C, Alonso JC (2015) DisA and c-di-AMP act at the intersection between DNA-damage response and stress homeostasis in exponentially growing Bacillus subtilis cells. DNA Repair (Amst) 27:1–8.  https://doi.org/10.1016/j.dnarep.2014.12.007 CrossRefGoogle Scholar
  72. 72.
    Zheng C, Ma Y, Wang X, Xie Y, Ali MK, He J (2015) Functional analysis of the sporulation-specific diadenylate cyclase CdaS in Bacillus thuringiensis. Front Microbiol 6:908.  https://doi.org/10.3389/fmicb.2015.00908 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Mehne FMP, Schröder-Tittmann K, Eijlander RT, Herzberg C, Hewitt L, Kaever V, Lewis RJ, Kuipers OP, Tittmann K, Stülke J (2014) Control of the diadenylate cyclase CdaS in Bacillus subtilis. J Biol Chem 289:21098–21107.  https://doi.org/10.1074/jbc.M114.562066 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Luo Y, Helmann JD (2012) A σD-dependent antisense transcript modulates expression of the cyclic-di-AMP hydrolase GdpP in Bacillus subtilis. Microbiology 158:2732–2741.  https://doi.org/10.1099/mic.0.062174-0 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Chai Y, Kolter R, Losick R (2010) Reversal of an epigenetic switch governing cell chaining in Bacillus subtilis by protein instability. Mol Microbiol 78:218–229.  https://doi.org/10.1111/j.1365-2958.2010.07335.x CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422.  https://doi.org/10.1146/annurev.micro.61.080706.093316 CrossRefPubMedGoogle Scholar
  77. 77.
    Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663.  https://doi.org/10.1111/1574-6976.12028 CrossRefPubMedGoogle Scholar
  78. 78.
    Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556.  https://doi.org/10.1146/annurev.micro.62.081307.162918 CrossRefPubMedGoogle Scholar
  79. 79.
    Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 13:848–864.  https://doi.org/10.1016/j.surg.2006.10.010.Use CrossRefGoogle Scholar
  80. 80.
    Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209.  https://doi.org/10.1007/s11104-004-5047-x CrossRefGoogle Scholar
  81. 81.
    Zhang H, Kim M-S, Sun Y, Dowd SE, Shi H, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant-Microbe Interact 21:737–744.  https://doi.org/10.1094/MPMI-21-6-0737 CrossRefPubMedGoogle Scholar
  82. 82.
    Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331.  https://doi.org/10.1111/1462-2920.12439 CrossRefPubMedGoogle Scholar
  83. 83.
    Woodward JJ, Iavarone AT, Portnoy DA (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703–1705.  https://doi.org/10.1126/science.1189801 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Yang J, Bai Y, Zhang Y, Gabrielle VD, Jin L, Bai G (2014) Deletion of the cyclic di-AMP phosphodiesterase gene (cnpB) in Mycobacterium tuberculosis leads to reduced virulence in a mouse model of infection. Mol Microbiol 93:65–79.  https://doi.org/10.1111/mmi.12641 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Barker JR, Koestler BJ, Carpenter VK, Burdette DL, Waters CM, Vance RE, Valdivia RH (2013) STING-Dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio 4:e00018–e00013.  https://doi.org/10.1128/mBio.00018-13 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Gries CM, Bruger EL, Moormeier DE, Scherr TD, Waters CM, Kielian T (2016) Cyclic di-AMP released from Staphylococcus aureus biofilm induces a macrophage type I interferon response. Infect Immun 84:3564–3574.  https://doi.org/10.1128/IAI.00447-16 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Nai C, Meyer V (2018) From axenic to mixed cultures: technological advances accelerating a paradigm shift in microbiology. Trends Microbiol 26:538–554.  https://doi.org/10.1016/j.tim.2017.11.004 CrossRefPubMedGoogle Scholar
  88. 88.
    Shank EA, Klepac-Ceraj V, Collado-Torres L, Powers GE, Losick R, Kolter R (2011) Interspecies interactions that result in Bacillus subtilis forming biofilms are mediated mainly by members of its own genus. Proc Natl Acad Sci 108:E1236–E1243.  https://doi.org/10.1073/pnas.1103630108 CrossRefPubMedGoogle Scholar
  89. 89.
    Teh WK, Dramsi S, Tolker-Nielsen T, Yang L, Givskov M (2019) Increased intracellular cyclic-di-AMP levels sensitize Streptococcus gallolyticus subsp. gallolyticus to osmotic stress, and reduce biofilm formation and adherence on intestinal cells. J Bacteriol 201:e00597–e00518.  https://doi.org/10.1128/JB.00597-18 CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Chen L, Li X, Zhou X, Zeng J, Ren Z, Lei L, Kang D, Zhang K, Zou J, Li Y (2018) Inhibition of Enterococcus faecalis growth and biofilm formation by molecule targeting cyclic di-AMP synthetase activity. J Endod 44:1381–1388.  https://doi.org/10.1016/j.joen.2018.05.008 CrossRefPubMedGoogle Scholar
  91. 91.
    Peng X, Zhang Y, Bai G, Zhou X, Wu H (2016) Cyclic di-AMP mediates biofilm formation. Mol Microbiol 99:945–959.  https://doi.org/10.1111/mmi.13277 CrossRefPubMedGoogle Scholar
  92. 92.
    Corrigan RM, Abbott JC, Burhenne H, Kaever V, Gründling A (2011) c-di-AMP Is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog 7:e1002217.  https://doi.org/10.1371/journal.ppat.1002217 CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Veličković D, Anderton CR (2017) Mass spectrometry imaging: towards mapping the elemental and molecular composition of the rhizosphere. Rhizosphere 3:254–258.  https://doi.org/10.1016/j.rhisph.2017.03.003 CrossRefGoogle Scholar
  94. 94.
    Garg N, Zeng Y, Edlund A, Melnik AV, Sanchez LM, Mohimani H, Gurevich A, Miao V, Schiffler S, Lim YW, Luzzatto-Knaan T, Cai S, Rohwer F, Pevzner PA, Cichewicz RH, Alexandrov T, Dorrestein PC (2016) Spatial molecular architecture of the microbial community of a Peltigera lichen. mSystems 1:e00139–e00116.  https://doi.org/10.1128/mSystems.00139-16 CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Valm AM, Mark Welch JL, Borisy GG (2012) CLASI-FISH: principles of combinatorial labeling and spectral imaging. Syst Appl Microbiol 35:496–502.  https://doi.org/10.1016/j.syapm.2012.03.004 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Valm AM, Oldenbourg R, Borisy GG (2016) Multiplexed spectral imaging of 120 different fluorescent labels. PLoS One 11:e0158495.  https://doi.org/10.1371/journal.pone.0158495 CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Peredo EL, Simmons SL (2018) Leaf-FISH: microscale imaging of bacterial taxa on phyllosphere. Front Microbiol 8:2669.  https://doi.org/10.3389/fmicb.2017.02669 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Sarah M. Yannarell
    • 1
    • 2
  • Loni Townsley
    • 2
  • Elizabeth A. Shank
    • 1
    • 2
    Email author
  1. 1.Department of Microbiology and ImmunologyUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Department of BiologyUniversity of North Carolina at Chapel HillChapel HillUSA

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