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Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system

  • 1.

    Muok AR, Briegel A. Intermicrobial hitchhiking: how nonmotile microbes leverage communal motility. Trends Microbiol. 2021;29:542–50.

    CAS 
    PubMed 

    Google Scholar 

  • 2.

    Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY. Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol. 2005;39:4640–6.

    CAS 
    PubMed 

    Google Scholar 

  • 3.

    Simon A, Bindschedler S, Job D, Wick LY, Filippidou S, Kooli WM, et al. Exploiting the fungal highway: development of a novel tool for the in situ isolation of bacteria migrating along fungal mycelium. FEMS Microbiol Ecol. 2015;91:fiv116.

    PubMed 

    Google Scholar 

  • 4.

    Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, et al. Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev. 2018;42:335–52.

    CAS 
    PubMed 

    Google Scholar 

  • 5.

    Harms H, Schlosser D, Wick LY. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol. 2011;9:177.

    CAS 
    PubMed 

    Google Scholar 

  • 6.

    Otten W, Hall D, Harris K, Ritz K, Young IM, Gilligan CA. Soil physics, fungal epidemiology and the spread of Rhizoctonia solani. N. Phytol. 2001;151:459–68.

    Google Scholar 

  • 7.

    Sun B, Chen X, Zhang X, Liang A, Whalen JK, McLaughlin NB. Greater fungal and bacterial biomass in soil large macropores under no-tillage than mouldboard ploughing. Eur J Soil Biol. 2020;97:103155.

    CAS 

    Google Scholar 

  • 8.

    Otto S, Bruni EP, Harms H, Wick LY. Catch me if you can: dispersal and foraging of Bdellovibrio bacteriovorus 109J along mycelia. ISME J. 2017;11:386–93.

    PubMed 

    Google Scholar 

  • 9.

    Kjeldgaard B, Listian SA, Ramaswamhi V, Richter A, Kiesewalter HT, Kovács ÁT. Fungal hyphae colonization by Bacillus subtilis relies on biofilm matrix components. Biofilm. 2019;1:100007.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Narr A, Nawaz A, Wick LY, Harms H, Chatzinotas A. Soil viral communities vary temporally and along a land use transect as revealed by virus-like particle counting and a modified community fingerprinting approach (fRAPD). Front Microbiol. 2017;8:1975.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 11.

    Rosner A, Gutstein R. Adsorption of actinophage Pal 6 to developing mycelium of Streptomyces albus. Can J Microbiol. 1981;27:254–7.

    CAS 
    PubMed 

    Google Scholar 

  • 12.

    Ghanem N, E. Stanley C, Harms H, Chatzinotas A,Y, Wick L. Mycelial effects on phage retention during transport in a microfluidic platform. Environ Sci Technol. 2019;53:11755–63.

    CAS 
    PubMed 

    Google Scholar 

  • 13.

    Dennehy JJ. What ecologists can tell virologists. Annu Rev Microbiol. 2014;68:117–35.

    CAS 
    PubMed 

    Google Scholar 

  • 14.

    Hurst CJ, Gerba CP, Cech I. Effects of environmental variables and soil characteristics on virus survival in soil. Appl Environ Microbiol. 1980;40:1067–79.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Yeager JG, Brien RT. Enterovirus inactivation in soil. Appl Environ Microbiol. 1979;38:694–701.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 16.

    Schwartz DA, Lindell D. Genetic hurdles limit the arms race between Prochlorococcus and the T7-like podoviruses infecting them. ISME J. 2017;11:1836–51.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Shan J, Ramachandran A, Thanki AM, Vukusic FBI, Barylski J, Clokie MRJ. Bacteriophages are more virulent to bacteria with human cells than they are in bacterial culture; insights from HT-29 cells. Sci Rep. 2018;8:5091.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 18.

    Chaudhry W, Lee E, Worthy A, Weiss Z, Grabowicz M, Vega NM, et al. Mucoidy, a general mechanism for maintaining lytic phage in populations of bacteria. FEMS Microbiology Ecology. 2020;96:fiaa162.

  • 19.

    Yu Z, Schwarz C, Zhu L, Chen L, Shen Y, Yu P. Hitchhiking behavior in bacteriophages facilitates phage infection and enhances carrier bacteria colonization. Environ Sci Technol. 2020;55:2462–72.

    PubMed 

    Google Scholar 

  • 20.

    Tarafder AK, von Kügelgen A, Mellul AJ, Schulze U, Aarts DGAL, Bharat TAM. Phage liquid crystalline droplets form occlusive sheaths that encapsulate and protect infectious rod-shaped bacteria. Proc Natl Acad Sci. 2020;117:4724–31.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 21.

    Callaway RM, Ridenour WM. Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ. 2004;2:436–43.

    Google Scholar 

  • 22.

    Granato ET, Meiller-Legrand TA, Foster KR. The evolution and ecology of bacterial warfare. Curr Biol. 2019;29:521–37.

    Google Scholar 

  • 23.

    Gama JA, Reis AM, Domingues I, Mendes-Soares H, Matos AM, Dionisio F. Temperate Bacterial viruses as double-edged swords in bacterial warfare. PLoS One. 2013;8:e59043.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 24.

    Dragoš A, Andersen AJC, Lozano-Andrade CN, Kempen PJ, Kovács ÁT, Strube ML. Phages carry interbacterial weapons encoded by biosynthetic gene clusters. Curr Biol. 2021;31:3479–89.

    PubMed 

    Google Scholar 

  • 25.

    Pyšek P, Bacher S, Kühn I, Novoa A, Catford JA, Hulme PE, et al. Macroecological framework for invasive aliens (MAFIA): disentangling large-scale context dependence in biological invasions. NeoBiota. 2020;62:407–61.

    Google Scholar 

  • 26.

    Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, et al. A proposed unified framework for biological invasions. Trends Ecol Evol. 2011;26:333–9.

    PubMed 

    Google Scholar 

  • 27.

    Richardson DM, Pyšek P. Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr Earth Environ. 2006;30:409–31.

    Google Scholar 

  • 28.

    Williamson M. Explaining and predicting the success of invading species at different stages of invasion. Biol Invasions. 2006;8:1561–8.

    Google Scholar 

  • 29.

    Demerec M, Adelberg EA, Clark AJ, Hartman PE. A proposal for a uniform nomenclature in bacterial genetics. Genetics 1966;54:61–76.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Dechesne A, Wang G, Gülez G, Or D, Smets BF. Hydration-controlled bacterial motility and dispersal on surfaces. Proc Natl Acad Sci. 2010;107:14369–72.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Maurhofer M, Keel C, Schnider U, Voisard C, Haas D, Defao G. Influence of enhanced antibiotic production in Pseudomanas fluorescens strain CHA0 on its disease suppressive capacity. Phytopathol. 1992;82:190–5.

    CAS 

    Google Scholar 

  • 32.

    Schamfuß S, Neu TR, van der Meer JR, Tecon R, Harms H, Wick LY. Impact of mycelia on the accessibility of fluorene to PAH-degrading bacteria. Environ Sci Technol. 2013;47:6908–15.

    PubMed 

    Google Scholar 

  • 33.

    Bichet MC, Chin WH, Richards W, Lin Y-W, Avellaneda-Franco L, Hernandez CA, et al. Bacteriophage uptake by mammalian cell layers represents a potential sink that may impact phage therapy. iScience. 2021;24:102287.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Lu F, Wu S-H, Hung Y, Mou C-Y. Size effect on cell uptake in well-suspended, uniform mesoporous silica nanoparticles. Small. 2009;5:1408–13.

    CAS 
    PubMed 

    Google Scholar 

  • 35.

    Fortier L-C, Moineau S Phage production and maintenance of stocks, including expected stock Lifetimes. In: Clokie MRJ, Kropinski AM, editors. Bacteriophages: Methods and Protocols, Volume 1: Isolation, Characterization, and Interactions. Totowa: Humana Press; 2009. p. 203–19.

  • 36.

    Mazzocco A, Waddell TE, Lingohr E, Johnson RP Enumeration of Bacteriophages Using the Small Drop Plaque Assay System In: Clokie MRJ, Kropinski AM, editors. Bacteriophages: Methods and Protocols, Volume 1: Isolation, Characterization, and Interactions Totowa: Humana Press; 2009. p. 81–85.

  • 37.

    Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP Enumeration of Bacteriophages by Double Agar Overlay Plaque Assay In: Clokie MRJ, Kropinski AM, editors. Bacteriophages: Methods and Protocols, Volume 1: Isolation, Characterization, and Interactions. Totowa: Humana Press; 2009. p. 69–76.

  • 38.

    Thanki AM, Taylor-Joyce G, Dowah A, Yakubu Nale J, Malik D, Rebecca Jane Clokie M. Unravelling the Links between Phage Adsorption and Successful Infection in Clostridium difficile. Viruses. 2018;10:441.

  • 39.

    Nair RR, Fiegna F, Velicer GJ. Indirect evolution of social fitness inequalities and facultative social exploitation. Proc R Soc B Biol Sci. 2018;285:20180054.

    Google Scholar 

  • 40.

    Postma M, Goedhart J. PlotsOfData—A web app for visualizing data together with their summaries. PLOS Biol. 2019;17:e3000202.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 41.

    Wood M. Statistical inference using bootstrap confidence intervals. Significance. 2004;1:180–2.

    Google Scholar 

  • 42.

    Cumming G, Finch S. Inference by eye: confidence interval and how to read pictures of data. Am Psychol. 2005;60:170–80.

    PubMed 

    Google Scholar 

  • 43.

    Frada MJ, Schatz D, Farstey V, Ossolinski JE, Sabanay H, Ben-Dor S, et al. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr Biol. 2014;24:2592–7.

    CAS 
    PubMed 

    Google Scholar 

  • 44.

    Frada MJ, Vardi A. Algal viruses hitchhiking on zooplankton across phytoplankton blooms. Commun Integr Biol. 2015;8:e1029210.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Totsche KU, Kögel-Knabner I. Mobile organic sorbent affected contaminant transport in soil: numerical case studies for enhanced and reduced mobility. Vadose Zo J. 2004;3:352–67.

    CAS 

    Google Scholar 

  • 46.

    Reche I, D’Orta G, Mladenov N, Winget DM, Suttle CA. Deposition rates of viruses and bacteria above the atmospheric boundary layer. ISME J. 2018;12:1154–62.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Lehmann K, Lehmann R, Totsche KU. Event-driven dynamics of the total mobile inventory in undisturbed soil account for significant fluxes of particulate organic carbon. Sci Total Environ. 2021;756:143774.

    CAS 
    PubMed 

    Google Scholar 

  • 48.

    Storms ZJ, Sauvageau D. Modeling tailed bacteriophage adsorption: insight into mechanisms. Virology. 2015;485:355–62.

    CAS 
    PubMed 

    Google Scholar 

  • 49.

    Shan Y, Harms H, Wick LY. Electric field effects on bacterial deposition and transport in porous media. Environ Sci Technol. 2018;52:14294–301.

    CAS 
    PubMed 

    Google Scholar 

  • 50.

    Junier P, Cailleau G, Palmieri I, Vallotton C, Trautschold OC, Junier T, et al. Democratization of fungal highway columns as a tool to investigate bacteria associated with soil fungi. FEMS Microbiol Ecol. 2021;97:fiab003.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 51.

    Furuno S, Remer R, Chatzinotas A, Harms H, Wick LY. Use of mycelia as paths for the isolation of contaminant-degrading bacteria from soil. Micro Biotechnol. 2012;5:142–8.

    CAS 

    Google Scholar 

  • 52.

    Jiang F, Zhang L, Zhou J, George TS, Feng G. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. N. Phytol. 2021;230:304–15.

    CAS 

    Google Scholar 

  • 53.

    Jansa J, Hodge A. Swimming, gliding, or hyphal riding? On microbial migration along the arbuscular mycorrhizal hyphal highway and functional consequences thereof. N. Phytol. 2021;230:14–16.

    Google Scholar 

  • 54.

    Zhang Y, Kastman EK, Guasto JS, Wolfe BE. Fungal networks shape dynamics of bacterial dispersal and community assembly in cheese rind microbiomes. Nat Commun. 2018;9:336.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 55.

    Ping D, Wang T, Fraebel DT, Maslov S, Sneppen K, Kuehn S. Hitchhiking, collapse, and contingency in phage infections of migrating bacterial populations. ISME J 2020;14:2007–18.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 56.

    Testa S, Berger S, Piccardi P, Oechslin F, Resch G, Mitri S. Spatial structure affects phage efficacy in infecting dual-strain biofilms of Pseudomonas aeruginosa. Commun Biol. 2019;2:405.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    May T, Tsuruta K, Okabe S. Exposure of conjugative plasmid carrying Escherichia coli biofilms to male-specific bacteriophages. ISME J. 2011;5:771–5.

    CAS 
    PubMed 

    Google Scholar 

  • 58.

    Abedon ST. Phage “delay” towards enhancing bacterial escape from biofilms: a more comprehensive way of viewing resistance to bacteriophages. AIMS Microbiol. 2017;3:186.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Adams MH Bacteriophages (Interscience Publishers, Inc., New York – London, 1959)

  • 60.

    Schrader HS, Schrader JO, Walker JJ, Bruggeman NB, Vanderloop JM, Shaffer JJ, et al. Effects of host starvation on bacteriophage dynamics. Bact Oligotrophic Environ Starvation-Survival Lifestyle. 1997; 368-85.

  • 61.

    Schrader HS, Schrader JO, Walker JJ, Wolf TA, Nickerson KW, Kokjohn TA. Bacteriophage infection and multiplication occur in Pseudomonas aeruginosa starved for 5 years. Can J Microbiol. 1997;43:1157–63.

    CAS 
    PubMed 

    Google Scholar 

  • 62.

    Łoś M, Golec P, Łoś JM, Węglewska-Jurkiewicz A, Czyż A, Węgrzyn A, et al. Effective inhibition of lytic development of bacteriophages λ, P1 and T4 by starvation of their host, Escherichia coli. BMC Biotechnol. 2007;7:13.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 63.

    Bryan D, El-Shibiny A, Hobbs Z, Porter J, Kutter EM. Bacteriophage T4 infection of stationary phase E. coli: life after log from a phage perspective. Front Microbiol. 2016;7:1391.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Yin J. A quantifiable phenotype of viral propagation. Biochem Biophys Res Commun. 1991;174:1009–14.

    CAS 
    PubMed 

    Google Scholar 

  • 65.

    Chatterjee A, Willett JLE, Dunny GM, Duerkop BA. Phage infection and sub-lethal antibiotic exposure mediate Enterococcus faecalis type VII secretion system dependent inhibition of bystander bacteria. PLOS Genet. 2021;17:e1009204.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Berthold T, Centler F, Hübschmann T, Remer R, Thullner M, Harms H, et al. Mycelia as a focal point for horizontal gene transfer among soil bacteria. Sci Rep. 2016;6:36390.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Lee KL, Hubbard LC, Hern S, Yildiz I, Gratzl M, Steinmetz NF. Shape matters: the diffusion rates of TMV rods and CPMV icosahedrons in a spheroid model of extracellular matrix are distinct. Biomater Sci. 2013;1. https://doi.org/10.1039/C3BM00191A.

  • 68.

    Hudson P, Greenman J. Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol. 1998;13:387–90.

    CAS 
    PubMed 

    Google Scholar 

  • 69.

    Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, et al. Ecological and evolutionary insights from species invasions. Trends Ecol Evol. 2007;22:465–71.

    PubMed 

    Google Scholar 

  • 70.

    Wagner PL, Waldor MK. Bacteriophage control of bacterial virulence. Infect Immun. 2020;70:3985–93.

    Google Scholar 

  • 71.

    Chantrey J, Dale TD, Read JM, White S, Whitfield F, Jones D, et al. European red squirrel population dynamics driven by squirrelpox at a gray squirrel invasion interface. Ecol Evol. 2014;4:3788–99.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 72.

    Essl F, Bacher S, Genovesi P, Hulme PE, Jeschke JM, Katsanevakis S, et al. Which taxa are alien? Criteria, applications, and uncertainties. Bioscience 2018;68:496–509.

    Google Scholar 

  • 73.

    Seebens H, Gastner MT, Blasius B. The risk of marine bioinvasion caused by global shipping. Ecol Lett. 2013;16:782–90.

    CAS 
    PubMed 

    Google Scholar 

  • 74.

    Seebens H, Essl F, Blasius B. The intermediate distance hypothesis of biological invasions. Ecol Lett. 2017;20:158–65.

    PubMed 

    Google Scholar 

  • 75.

    Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, et al. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol. 2008;45:403–14.

    Google Scholar 

  • 76.

    Liebhold AM, Brockerhoff EG, Garrett LJ, Parke JL, Britton KO. Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ. 2012;10:135–43.

    Google Scholar 


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