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An Eco-evolutionary Model on Surviving Lysogeny Through Grounding and Accumulation of Prophages

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Abstract

Temperate phages integrate into the bacterial genomes propagating along with the bacterial genomes. Multiple phage elements, representing diverse prophages, are present in most bacterial genomes. The evolutionary events and the ecological dynamics underlying the accumulation of prophage elements in bacterial genomes have yet to be understood. Here, we show that the local wastewater had 7% of lysogens (hosting mitomycin C-inducible prophages), and they showed resistance to superinfection by their corresponding lysates. Genomic analysis of four lysogens and four non-lysogens revealed the presence of multiple prophages (belonging to Myoviridae and Siphoviridae) in both lysogens and non-lysogens. For large-scale comparison, 2180 Escherichia coli genomes isolated from various sources across the globe and 523 genomes specifically isolated from diverse wastewaters were analyzed. A total of 15,279 prophages were predicted among 2180 E. coli genomes and 2802 prophages among 523 global wastewater isolates, with a mean of ~ 5 prophages per genome. These observations indicate that most putative prophages are relics of past bacteria-phage conflicts; they are “grounded” prophages that cannot excise from the bacterial genome. Prophage distribution analysis based on the sequence homology suggested the random distribution of E. coli prophages within and between E. coli clades. The independent occurrence pattern of these prophages indicates extensive horizontal transfers across the genomes. We modeled the eco-evolutionary dynamics to reconstruct the events that could have resulted in the prophage accumulation accounting for infection, superinfection immunity, and grounding. In bacteria-phage conflicts, the bacteria win by grounding the prophage, which could confer superinfection immunity.

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Data Availability

All data generated or analyzed during this study are included in this published article (and its supplementary information files) and deposited at NCBI with the BioProject ID PRJNA843888. The Python source code used for modeling studies can be found at https://github.com/Pavi31/Bacteria_Phage_dynamics.git.

References

  1. Harrison E, Brockhurst MA (2017) Ecological and evolutionary benefits of temperate phage: what does or doesn’t kill you makes you stronger. BioEssays: News Rev Mole Cell Dev Biol 39:1700112. https://doi.org/10.1002/bies.201700112

    Article  Google Scholar 

  2. Bruce JB, Lion S, Buckling A, Westra ER, Gandon S (2021) Regulation of prophage induction and lysogenization by phage communication systems. Curr Biol : CB 31(5046–5051):e5047. https://doi.org/10.1016/j.cub.2021.08.073

    Article  CAS  Google Scholar 

  3. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317. https://doi.org/10.1038/nrmicro2315

    Article  CAS  PubMed  Google Scholar 

  4. Silveira CB, Rohwer FL (2016) Piggyback-the-Winner in host-associated microbial communities. NPJ Biofilms Microbiomes 2:16010. https://doi.org/10.1038/npjbiofilms.2016.10

    Article  PubMed  PubMed Central  Google Scholar 

  5. Berngruber TW, Weissing FJ, Gandon S (2010) Inhibition of superinfection and the evolution of viral latency. J Virol 84:10200–10208. https://doi.org/10.1128/JVI.00865-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Shabbir MA, Hao H, Shabbir MZ, Wu Q, Sattar A, Yuan Z (2016) Bacteria vs. bacteriophages: parallel evolution of immune arsenals. Front Microbiol 7:1292. https://doi.org/10.3389/fmicb.2016.01292

    Article  PubMed  PubMed Central  Google Scholar 

  7. Koskella B, Brockhurst MA (2014) Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38:916–931. https://doi.org/10.1111/1574-6976.12072

    Article  CAS  PubMed  Google Scholar 

  8. Grange JM, Krone B, Kolmel K (2005) Human endogenous retroviruses in health and disease. J R Soc Med 98:134. https://doi.org/10.1177/014107680509800318

    Article  PubMed  PubMed Central  Google Scholar 

  9. Dopkins N, O’Mara MM, Singh B, Marston JL, Bendall ML, Nixon DF (2022) How human endogenous retroviruses interact with the microbiota in health and disease. Trends Microbiol 30:812–815. https://doi.org/10.1016/j.tim.2022.05.011

    Article  CAS  PubMed  Google Scholar 

  10. Mirzaei MK, Maurice CF (2017) Menage a trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol 15:397–408. https://doi.org/10.1038/nrmicro.2017.30

    Article  CAS  PubMed  Google Scholar 

  11. Tang X, Fan C, Zeng G, Zhong L, Li C, Ren X, Song B, Liu X (2022) Phage-host interactions: the neglected part of biological wastewater treatment. Water Res 226:119183. https://doi.org/10.1016/j.watres.2022.119183

    Article  CAS  PubMed  Google Scholar 

  12. Lood R, Erturk G, Mattiasson B (2017) Revisiting antibiotic resistance spreading in wastewater treatment plants - bacteriophages as a much neglected potential transmission vehicle. Front Microbiol 8:2298. https://doi.org/10.3389/fmicb.2017.02298

    Article  PubMed  PubMed Central  Google Scholar 

  13. Raya RR, HeBert EM (2009) Isolation of phage via induction of lysogens. Methods Mol Biol 501:23–32. https://doi.org/10.1007/978-1-60327-164-6_3

    Article  CAS  PubMed  Google Scholar 

  14. Lobova TI, Feil EJ, Popova LY (2011) Multiple antibiotic resistance of heterotrophic bacteria isolated from Siberian lakes subjected to differing degrees of anthropogenic impact. Microb Drug Resist 17:583–591. https://doi.org/10.1089/mdr.2011.0044

    Article  CAS  PubMed  Google Scholar 

  15. Antonopoulos DA, Assaf R, Aziz RK, Brettin T, Bun C, Conrad N, Davis JJ, Dietrich EM, Disz T, Gerdes S, Kenyon RW, Machi D, Mao C, Murphy-Olson DE, Nordberg EK, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Santerre J, Shukla M, Stevens RL, VanOeffelen M, Vonstein V, Warren AS, Wattam AR, Xia F, Yoo H (2019) PATRIC as a unique resource for studying antimicrobial resistance. Brief Bioinform 20:1094–1102. https://doi.org/10.1093/bib/bbx083

    Article  CAS  PubMed  Google Scholar 

  16. Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G (2010) Interactive microbial genome visualization with GView. Bioinformatics 26:3125–3126. https://doi.org/10.1093/bioinformatics/btq588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Reis-Cunha JL, Bartholomeu DC, Manson AL, Earl AM, Cerqueira GC (2019) ProphET, prophage estimation tool: a stand-alone prophage sequence prediction tool with self-updating reference database. PLoS One 14:e0223364. https://doi.org/10.1371/journal.pone.0223364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153

    Article  CAS  PubMed  Google Scholar 

  19. Nishimura Y, Yoshida T, Kuronishi M, Uehara H, Ogata H, Goto S (2017) ViPTree: the viral proteomic tree server. Bioinformatics 33:2379–2380. https://doi.org/10.1093/bioinformatics/btx157

    Article  CAS  PubMed  Google Scholar 

  20. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, Chlenski P, Conrad N, Dickerman A, Dietrich EM, Gabbard JL, Gerdes S, Guard A, Kenyon RW, Machi D, Mao C, Murphy-Olson D, Nguyen M, Nordberg EK, Olsen GJ, Olson RD, Overbeek JC, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomas C, VanOeffelen M, Vonstein V, Warren AS, Xia F, Xie D, Yoo H, Stevens R (2020) The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities. Nucleic Acids Res 48:D606–D612. https://doi.org/10.1093/nar/gkz943

    Article  CAS  PubMed  Google Scholar 

  21. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O (2018) ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microbial Genomics 4(7):e000192. https://doi.org/10.1099/mgen.0.000192

    Article  PubMed  PubMed Central  Google Scholar 

  22. Sudhakari PA, Ramisetty BCM (2022) Modeling endonuclease colicin-like bacteriocin operons as ‘genetic arms’ in plasmid-genome conflicts. Mol Gen Genomics : MGG 297:763–777. https://doi.org/10.1007/s00438-022-01884-4

    Article  CAS  Google Scholar 

  23. Gama JA, Reis AM, Domingues I, Mendes-Soares H, Matos AM, Dionisio F (2013) Temperate bacterial viruses as double-edged swords in bacterial warfare. PLoS One 8:e59043. https://doi.org/10.1371/journal.pone.0059043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cortes MG, Krog J, Balazsi G (2019) Optimality of the spontaneous prophage induction rate. J Theor Biol 483:110005. https://doi.org/10.1016/j.jtbi.2019.110005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Cheong KH, Wen T, Benler S, Koh JM, Koonin EV (2022) Alternating lysis and lysogeny is a winning strategy in bacteriophages due to Parrondo’s paradox. Proc Natl Acad Sci U S A 119:e2115145119. https://doi.org/10.1073/pnas.2115145119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhu Y, Shang J, Peng C, Sun Y (2022) Phage family classification under Caudoviricetes: a review of current tools using the latest ICTV classification framework. Front Microbiol 13:1032186. https://doi.org/10.3389/fmicb.2022.1032186

    Article  PubMed  PubMed Central  Google Scholar 

  27. Dion MB, Oechslin F, Moineau S (2020) Phage diversity, genomics and phylogeny. Nat Rev Microbiol. https://doi.org/10.1038/s41579-019-0311-5

    Article  PubMed  Google Scholar 

  28. Moreno-Gallego JL, Chou SP, Di Rienzi SC, Goodrich JK, Spector TD, Bell JT, Youngblut ND, Hewson I, Reyes A, Ley RE (2019) Virome diversity correlates with intestinal microbiome diversity in adult monozygotic twins. Cell Host Microbe 25(261–272):e265. https://doi.org/10.1016/j.chom.2019.01.019

    Article  CAS  Google Scholar 

  29. Chibani CM, Farr A, Klama S, Dietrich S, Liesegang H (2019) Classifying the unclassified: a phage classification method. Viruses 11(2):195. https://doi.org/10.3390/v11020195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I, Herskovits AA (2015) A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13:641. https://doi.org/10.1038/nrmicro3527

    Article  CAS  PubMed  Google Scholar 

  31. Greenrod STE, Stoycheva M, Elphinstone J, Friman VP (2022) Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex. BMC Genomics 23:689. https://doi.org/10.1186/s12864-022-08909-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ramisetty BCM, Sudhakari PA (2019) Bacterial ‘grounded’ prophages: hotspots for genetic renovation and innovation. Front Genet 10:65. https://doi.org/10.3389/fgene.2019.00065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB (2017) Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J 11:1511–1520. https://doi.org/10.1038/ismej.2017.16

    Article  PubMed  PubMed Central  Google Scholar 

  34. Guo Z, Sloot PM, Tay JC (2008) A hybrid agent-based approach for modeling microbiological systems. J Theor Biol 255:163–175. https://doi.org/10.1016/j.jtbi.2008.08.008

    Article  CAS  PubMed  Google Scholar 

  35. Stewart FM, Levin BR (1984) The population biology of bacterial viruses: why be temperate. Theor Popul Biol 26:93–117. https://doi.org/10.1016/0040-5809(84)90026-1

    Article  CAS  PubMed  Google Scholar 

  36. Casjens SR (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8:451–458. https://doi.org/10.1016/j.mib.2005.06.014

    Article  CAS  PubMed  Google Scholar 

  37. Kim MS, Bae JW (2018) Lysogeny is prevalent and widely distributed in the murine gut microbiota. ISME J 12:1127–1141. https://doi.org/10.1038/s41396-018-0061-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann Y, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blocker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowki J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, Szustakowki J, International Human Genome Sequencing C (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921. https://doi.org/10.1038/35057062

    Article  CAS  PubMed  Google Scholar 

  39. Grandi N, Tramontano E (2018) Human endogenous retroviruses are ancient acquired elements still shaping innate immune responses. Front Immunol 9:2039. https://doi.org/10.3389/fimmu.2018.02039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Runa V, Wenk J, Bengtsson S, Jones BV, Lanham AB (2021) Bacteriophages in biological wastewater treatment systems: occurrence, characterization, and function. Front Microbiol 12:730071. https://doi.org/10.3389/fmicb.2021.730071

    Article  PubMed  PubMed Central  Google Scholar 

  41. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181. https://doi.org/10.1016/j.femsre.2003.08.001

    Article  CAS  PubMed  Google Scholar 

  42. Henrot C, Petit MA (2022) Signals triggering prophage induction in the gut microbiota. Mol Microbiol 118:494–502. https://doi.org/10.1111/mmi.14983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Canchaya C, Proux C, Fournous G, Bruttin A, Brussow H (2003) Prophage genomics. Microbiol Mol Biol Rev 67:238–276. https://doi.org/10.1128/mmbr.67.2.238-276.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Egido JE, Costa AR, Aparicio-Maldonado C, Haas PJ, Brouns SJJ (2022) Mechanisms and clinical importance of bacteriophage resistance. FEMS Microbiol Rev 46(1):fuab048. https://doi.org/10.1093/femsre/fuab048

  45. Hasan M, Ahn J (2022) Evolutionary dynamics between phages and bacteria as a possible approach for designing effective phage therapies against antibiotic-resistant bacteria. Antibiotics 11(7):915. https://doi.org/10.3390/antibiotics11070915

  46. Williams KP (2002) Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866–875. https://doi.org/10.1093/nar/30.4.866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Koonin EV (2016) Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 5(F1000 Faculty Rev):1805. https://doi.org/10.12688/f1000research.8737.1

  48. Wahl LM, Betti MI, Dick DW, Pattenden T, Puccini AJ (2019) Evolutionary stability of the lysis-lysogeny decision: why be virulent? Evolution 73:92–98. https://doi.org/10.1111/evo.13648

    Article  CAS  PubMed  Google Scholar 

  49. Monaco AP (2022) The selfish environment meets the selfish gene: coevolution and inheritance of RNA and DNA pools: a model for organismal life incorporating coevolution, horizontal transfer, and inheritance of internal and external RNA and DNA pools.: a model for organismal life incorporating coevolution, horizontal transfer, and inheritance of internal and external RNA and DNA pools. BioEssays : News Rev Mole Cell Dev Biol 44:e2100239. https://doi.org/10.1002/bies.202100239

    Article  CAS  Google Scholar 

  50. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL (2016) Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10:2854–2866. https://doi.org/10.1038/ismej.2016.79

    Article  PubMed  PubMed Central  Google Scholar 

  51. Mavrich TN, Hatfull GF (2019) Evolution of superinfection immunity in cluster A mycobacteriophages. mBio 10(3):e00971-19. https://doi.org/10.1128/mBio.00971-19

  52. Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, Sturino JM, Wood TK (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1:147. https://doi.org/10.1038/ncomms1146

    Article  CAS  PubMed  Google Scholar 

  53. Bergthorsson U, Ochman H (1998) Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol 15:6–16. https://doi.org/10.1093/oxfordjournals.molbev.a025847

    Article  CAS  PubMed  Google Scholar 

  54. Lawrence JG, Hendrix RW, Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends Microbiol 9:535–540. https://doi.org/10.1016/S0966-842X(01)02198-9

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We acknowledge the support from the System Analyst, L. Thiyagarajan, and the School of Computing at SASTRA Deemed University, for providing computing resources to run the simulations. We acknowledge Mr. S. V. Shridhar, Water Resource Supervisor, SASTRA Deemed University, for his support during sampling and related information.

Funding

This work was supported by Prof T. R. Rajagopalan grants (Internal funds) and the Central Research Facility sanctioned by SASTRA Deemed University, Thanjavur. P. A. S. is supported through the Senior Research Fellowship by the University Grants Commission (479/CSIR-UGC NET JUNE2019), Government of India.

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  1. Laboratory of Molecular Biology and Evolution, School of Chemical and Biotechnology, SASTRA Deemed University, 312@ASK1, Thanjavur, India

    Pavithra Anantharaman Sudhakari & Bhaskar Chandra Mohan Ramisetty

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B. C. M. R. conceived and designed the work. P. A. S. carried out the experiments, NGS data analyses, and bioinformatic analyses and prepared the figures. P. A. S. and B. C. M. R. interpreted the results and wrote the manuscripts.

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Correspondence to Bhaskar Chandra Mohan Ramisetty.

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Sudhakari, P.A., Ramisetty, B.C.M. An Eco-evolutionary Model on Surviving Lysogeny Through Grounding and Accumulation of Prophages. Microb Ecol 86, 3068–3081 (2023). https://doi.org/10.1007/s00248-023-02301-y

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