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Microbial Communication Networks: Sketching a Method for Analyzing the Communication of Bacteriophages Inside Environmental Communities

  • Charles Bernard
  • Philippe Lopez
  • Eric BaptesteEmail author
Chapter
  • 23 Downloads

Abstract

Recent functional studies have shed light into how the combinatorics of genes associated with quorum sensing (QS) – often described as an entity-entity communication mechanism – may support different communication modalities in bacteriophages. Specifically, only systems of QS genes for phage to phage communication and eavesdropping on bacterial communication molecules have been characterized so far, which represents only a fraction of the spectrum of all the possible communication modalities predicted by this combinatory logic. However, we argue that computational methods are already available to systematically mine the genomes of viruses and other microorganisms for QS genes, to compare these genes together across genomes, and to infer many novel links and types of communication between microbiological entities. All these putative communication links could be conveniently represented together in the form of a network, which would summarize which virus is suspected to interact with which microbiological entity, via which QS signaling molecule and foremost, under which communication modality. Besides, with the recent advents of metagenomics and metaviromics that enable accessing to genomes sequenced from the same environmental site, it would be theoretically possible to use this methodology to partially infer the big picture of communication inside a real community of viruses and cellular organisms. Finally, we discuss how the systematic analysis of such predicted microbial communication networks could provide insights into the many forms and “social” consequences that the biocommunication of viruses may imply.

References

  1. Abedon ST (2015) Bacteriophage secondary infection. Virol Sin 30(1):3–10.  https://doi.org/10.1007/s12250-014-3547-2CrossRefPubMedGoogle Scholar
  2. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31(6):533–538.  https://doi.org/10.1038/nbt.2579CrossRefPubMedGoogle Scholar
  3. Bhatt VS (2018) Quorum sensing mechanisms in gram positive bacteria, in implication of quorum sensing system in biofilm formation and virulence. Singapore, Springer Singapore, pp 297–311.  https://doi.org/10.1007/978-981-13-2429-1_20
  4. Blondel VD, Guillaume J-L, Lambiotte R, Lefebvre E (2008) Fast unfolding of communities in large networks. J Stat Mech: Theory Exp 2008(10):P10008.  https://doi.org/10.1088/1742-5468/2008/10/P10008CrossRefGoogle Scholar
  5. Bonacich P (1972) Factoring and weighting approaches to status scores and clique identification. J Math Sociol 2(1):113–120.  https://doi.org/10.1080/0022250X.1972.9989806CrossRefGoogle Scholar
  6. Bouttier J, Di Francesco P, Guitter E (2003) Geodesic distance in planar graphs. Nucl Phys B 663(3):535–567.  https://doi.org/10.1016/S0550-3213(03)00355-9CrossRefGoogle Scholar
  7. Breitwieser FP, Lu J, Salzberg SL (2019) A review of methods and databases for metagenomic classification and assembly. Brief Bioinform 20(4):1125–1136.  https://doi.org/10.1093/bib/bbx120CrossRefPubMedGoogle Scholar
  8. Corel E, Méheust R, Watson AK, McInerney JO, Lopez P, Bapteste E (2018) Bipartite network analysis of gene sharings in the microbial world. Mol Biol Evol 35(4):899–913.  https://doi.org/10.1093/molbev/msy001CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci U S A 111(11):4280–4284.  https://doi.org/10.1073/pnas.1319175111CrossRefPubMedPubMedCentralGoogle Scholar
  10. Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A, Peleg Y, Melamed S et al (2017) Communication between viruses guides lysis-lysogeny decisions. Nature 541(7638):488–493.  https://doi.org/10.1038/nature21049CrossRefPubMedPubMedCentralGoogle Scholar
  11. Freeman LC (1978) Centrality in social networks conceptual clarification. Soc Networks 1(3):215–239.  https://doi.org/10.1016/0378-8733(78)90021-7CrossRefGoogle Scholar
  12. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269–275.  https://doi.org/10.1128/jb.176.2.269-275.1994CrossRefPubMedPubMedCentralGoogle Scholar
  13. González JF, Venturi V (2013) A novel widespread interkingdom signaling circuit. Trends Plant Sci 18(3):167–174.  https://doi.org/10.1016/j.tplants.2012.09.007CrossRefPubMedGoogle Scholar
  14. Hargreaves KR, Kropinski AM, Clokie MRJ (2014) “What does the talking?: quorum sensing signalling genes discovered in a bacteriophage genome.” edited by Gunnar F. Kaufmann. PLoS One 9(1):e85131.  https://doi.org/10.1371/journal.pone.0085131CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hochstrasser R, Hilbi H (2017) Intra-species and inter-kingdom signaling of Legionella Pneumophila. Front Microbiol 8:79.  https://doi.org/10.3389/FMICB.2017.00079CrossRefPubMedPubMedCentralGoogle Scholar
  16. Johnson MR, Montero CI, Conners SB, Shockley KR, Bridger SL, Kelly RM (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga Maritima. Mol Microbiol 55(3):664–674.  https://doi.org/10.1111/j.1365-2958.2004.04419.xCrossRefPubMedGoogle Scholar
  17. Jung SA, Chapman CA, Ng W-L (2015) Quadruple quorum-sensing inputs control vibrio cholerae virulence and maintain system robustness. PLoS Pathog 11(4):e1004837.  https://doi.org/10.1371/journal.ppat.1004837CrossRefPubMedPubMedCentralGoogle Scholar
  18. Karavolos MH, Winzer K, Williams P, Anjam Khan CM (2013) Pathogen espionage: multiple bacterial adrenergic sensors eavesdrop on host communication systems. Mol Microbiol 87(3):455–465.  https://doi.org/10.1111/mmi.12110CrossRefPubMedGoogle Scholar
  19. Lee W, Lee S-H, Kim M, Moon J-S, Kim G-W, Jung H-G, Kim IH et al (2018) Vibrio Vulnificus quorum-sensing molecule cyclo(Phe-Pro) inhibits RIG-I-mediated antiviral innate immunity. Nat Commun 9(1):1606.  https://doi.org/10.1038/s41467-018-04075-1CrossRefPubMedPubMedCentralGoogle Scholar
  20. Luo C, Knight R, Siljander H, Knip M, Xavier RJ, Gevers D (2015) ConStrains identifies microbial strains in metagenomic datasets. Nat Biotechnol 33(10):1045–1052.  https://doi.org/10.1038/nbt.3319CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mehmood A, Liu G, Wang X, Meng G, Wang C, Liu Y (2019) Fungal quorum-sensing molecules and inhibitors with potential antifungal activity: a review. Molecules (Basel, Switzerland) 24(10).  https://doi.org/10.3390/molecules24101950
  22. Mehta P, Goyal S, Long T, Bassler BL, Wingreen NS (2009) Information processing and signal integration in bacterial quorum sensing. Mol Syst Biol 5(1):325.  https://doi.org/10.1038/msb.2009.79CrossRefPubMedPubMedCentralGoogle Scholar
  23. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55(1):165–199.  https://doi.org/10.1146/annurev.micro.55.1.165CrossRefPubMedGoogle Scholar
  24. Mukherjee S, Bassler BL (2019) Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol 17(6):371–382.  https://doi.org/10.1038/s41579-019-0186-5CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104(1):313–322CrossRefGoogle Scholar
  26. Newman MEJ (2005) A measure of betweenness centrality based on random walks. Soc Networks 27(1):39–54.  https://doi.org/10.1016/J.SOCNET.2004.11.009CrossRefGoogle Scholar
  27. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science (New York, NY) 325(5943):992–994.  https://doi.org/10.1126/science.1174463CrossRefGoogle Scholar
  28. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39(1):409–429.  https://doi.org/10.1146/annurev.genet.39.073003.113656CrossRefPubMedGoogle Scholar
  29. Paggi RA, Martone CB, Fuqua C, Castro RE (2003) Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus Occultus. FEMS Microbiol Lett 221(1):49–52.  https://doi.org/10.1016/S0378-1097(03)00174-5CrossRefPubMedGoogle Scholar
  30. Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in gram-negative bacteria. Nat Rev Microbiol 14(9):576–588.  https://doi.org/10.1038/nrmicro.2016.89CrossRefPubMedPubMedCentralGoogle Scholar
  31. Probst AJ, Ladd B, Jarett JK, Geller-McGrath DE, Sieber CMK, Emerson JB, Anantharaman K et al (2018) Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat Microbiol 3(3):328–336.  https://doi.org/10.1038/s41564-017-0098-yCrossRefPubMedPubMedCentralGoogle Scholar
  32. Rajput A, Kaur K, Kumar M (2016) SigMol: repertoire of quorum sensing signaling molecules in prokaryotes. Nucleic Acids Res 44(D1):D634–D639.  https://doi.org/10.1093/nar/gkv1076CrossRefPubMedGoogle Scholar
  33. Schuch R, Fischetti VA (2009) The secret life of the anthrax agent Bacillus Anthracis: bacteriophage-mediated ecological adaptations. PLoS One 4(8):e6532.  https://doi.org/10.1371/journal.pone.0006532CrossRefPubMedPubMedCentralGoogle Scholar
  34. Shaw ME (1954) Group structure and the behavior of individuals in small groups. J Psychol 38(1):139–149.  https://doi.org/10.1080/00223980.1954.9712925CrossRefGoogle Scholar
  35. Silpe JE, Bassler BL (2019a) A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Cell 176(1–2):268–280.e13.  https://doi.org/10.1016/J.CELL.2018.10.059CrossRefPubMedGoogle Scholar
  36. Silpe JE, Bassler BL (2019b) Phage-encoded LuxR-type receptors responsive to host-produced bacterial quorum-sensing autoinducers. BioRxiv March:577726.  https://doi.org/10.1101/577726CrossRefGoogle Scholar
  37. Stokar-Avihail A, Tal N, Erez Z, Lopatina A, Sorek R (2019) Widespread utilization of peptide communication in phages infecting soil and pathogenic bacteria. Cell Host Microbe 25(5):746–755.e5.  https://doi.org/10.1016/j.chom.2019.03.017CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sun J, Daniel R, Wagner-Döbler I, Zeng A-P (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4(1):36.  https://doi.org/10.1186/1471-2148-4-36CrossRefPubMedPubMedCentralGoogle Scholar
  39. Sztajer H, Szafranski SP, Tomasch J, Reck M, Nimtz M, Rohde M, Wagner-Döbler I (2014) Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus Mutans and Candida Albicans. ISME J 8(11):2256–2271.  https://doi.org/10.1038/ismej.2014.73CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wahl LM, Betti MI, Dick DW, Pattenden T, Puccini AJ (2018) Evolutionary stability of the lysis-lysogeny decision: why be virulent? Evolution 73(1):evo.13648.  https://doi.org/10.1111/evo.13648CrossRefGoogle Scholar
  41. Waters CM, Bassler BL (2005) QUORUM SENSING: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21(1):319–346.  https://doi.org/10.1146/annurev.cellbio.21.012704.131001CrossRefPubMedGoogle Scholar
  42. Watve S, Barrasso K, Jung SA, Davis KJ, Hawver LA, Khataokar A, Palaganas RG, Neiditch MB, Perez LJ, Ng W-L (2019) Ethanolamine regulates CqsR quorum-sensing signaling in vibrio cholerae. BioRxiv March:589390.  https://doi.org/10.1101/589390CrossRefGoogle Scholar
  43. Yang P, Yu S, Lin C, Ning K (2019) Meta-network: optimized species-species network analysis for microbial communities. BMC Genomics 20(S2):187.  https://doi.org/10.1186/s12864-019-5471-1CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhang G, Zhang F, Ding G, Li J, Guo X, Zhu J, Zhou L et al (2012) Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon. ISME J 6(7):1336–1344.  https://doi.org/10.1038/ismej.2011.203CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Charles Bernard
    • 1
    • 2
  • Philippe Lopez
    • 1
  • Eric Bapteste
    • 1
    Email author
  1. 1.Institut de Systématique, Evolution, Biodiversité (ISYEB)Sorbonne Université, CNRS, Museum National d’Histoire NaturelleParisFrance
  2. 2.Unité Molécules de Communication et Adaptation des Micro-organismes (MCAM), CNRS, Museum National d’Histoire NaturelleParisFrance

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