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Antimicrobials and the Natural Biology of a Bacterial-Nematode Symbiosis

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The Mechanistic Benefits of Microbial Symbionts

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 2))

Abstract

The Gram-negative proteobacterium, Xenorhabdus nematophila, engages in a mutualistic association with a nematode partner, Steinernema carpocapsae, which infects susceptible insect hosts. After entering the insect, the nematode carrying X. nematophila penetrates the intestine and enters the insect body cavity (hemocoel) where X. nematophila is released transitioning to its pathogenic stage. Together, X. nematophila and the nematode kill the insect host. Microbiota from the insect gut is assumed to translocate into the hemocoel during nematode invasion. In the hemocoel, X. nematophila encounters the dual challenge of inhibiting potential microbial competitors that may proliferate in the insect blood (hemolymph) and suppressing the host innate immune response. X. nematophila produces a plethora of small molecule antimicrobial compounds and secondary metabolites that function in interspecies competition and immune suppression. Suppressing growth of potential competitors and neutralizing an activated immune response not only benefit X. nematophila directly but also enhance fitness of the nematode that reproduces in the hemocoel. Thus, the secondary metabolites support a defensive mutualism between the bacterium and nematode. While secondary metabolites produced at high levels in broth culture can have antimicrobial properties in in vitro assays, their role in a natural infection of an insect host where they may be produced at subinhibitory concentrations is yet to be elucidated. In the present chapter, we discuss the diverse antimicrobial and immunosuppressive compounds produced by X. nematophila and their potential roles in this intriguing defensive mutualism and describe the microbial population dynamics in the hemocoel during the early phase of infection.

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References

  • Akhurst RJ (1980) Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J Gen Microbiol 121:303–309

    Google Scholar 

  • Akhurst RJ (1982) Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol 128:3061–3065

    CAS  PubMed  Google Scholar 

  • Alatorre-Rosas R, Kaya HK (1990) Interspecific competition between entomopathogenic nematodes in the Genera Heterorhabditis and Steinernema for an insect host in sand. J Invertebr Pathol 55:179–188

    Article  Google Scholar 

  • Bird A, Akhurst RJ (1983) The nature of the intestinal vesicle in nematodes of the family Steinernematidae. Int J Parasitol 13:599–606

    Article  Google Scholar 

  • Boemare N, Banifassi E, Laumond C et al (1983) Experimental study of the pathogenicity of Neoaplectana carpocapsae: Gnotobiotic studies in Galleria mellonella. Agronomie 3:407–415

    Article  Google Scholar 

  • Brachmann AO, Brameyer S, Kresovic D et al (2013) Pyrones as bacterial signaling molecules. Nat Chem Biol 9:573–578

    Article  CAS  PubMed  Google Scholar 

  • Calvo JM, Matthews RG (1994) The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol Rev 58:466–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell JF, Lewis E, Yoder F et al (1995) Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) seasonal population dynamics and impact on insect populations in turfgrass. Biol Control 5:598–606

    Article  Google Scholar 

  • Chaston JM, Suen G, Tucker SL et al (2011) The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes. PLoS One 6, e27909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaston JM, Murfin KE, Heath-Heckman EA et al (2013) Previously unrecognized stages of species-specific colonization in the mutualism between Xenorhabdus bacteria and Steinernema nematodes. Cell Microbiol 15:1545–1559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciche TA, Bintrim SB, Horswill AR et al (2001) A Phosphopantetheinyl transferase homolog is essential for Photorhabdus luminescens to support growth and reproduction of the entomopathogenic nematode Heterorhabditis bacteriophora. J Bacteriol 183:3117–3126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciche TA, Kim K-S, Kaufmann-Daszczuk B et al (2008) Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Appl Environ Microbiol 74:2275–2287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowles KN, Cowles CE, Richards GR et al (2007) The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol 9:1311–1323

    Article  CAS  PubMed  Google Scholar 

  • Crawford JM, Portmann C, Kontnik R et al (2011) NRPS substrate promiscuity diversifies the xenematides. Org Lett 13:5144–5147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford JM, Portmann C, Zhang X et al (2012) Small molecule perimeter defense in entomopathogenic bacteria. Proc Natl Acad Sci U S A 109:10821–10826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies J, Spiegelman GB, Yim G (2006) The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9:445–453

    Article  CAS  PubMed  Google Scholar 

  • Dietrich LE, Teal TK, Price-Whelan A et al (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drace K, Darby C (2008) The hmsHFRS operon of Xenorhabdus nematophila is required for biofilm attachment to Caenorhabditis elegans. Appl Environ Microbiol 74:4509–4515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eleftherianos I, Boundy S, Joyce SA et al (2007a) An antibiotic produced by an insect-pathogenic bacterium suppresses host defenses through phenoloxidase inhibition. Proc Natl Acad Sci U S A 104:2419–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eleftherianos I, Gokcen F, Felfoldi G et al (2007b) The immunoglobulin family protein Hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cell Microbiol 9:1137–1147

    Article  CAS  PubMed  Google Scholar 

  • Endo BY, Nickle WR (1995) Ultrastructure of anterior and midregions of infective juveniles of Steinernema feltiae. Fundam Appl Nematol 18:271–294

    Google Scholar 

  • Eom S, Park Y, Kim Y (2014) Sequential immunosuppressive activities of bacterial secondary metabolites from the entomopahogenic bacterium Xenorhabdus nematophila. J Microbiol 52:161–168

    Article  CAS  PubMed  Google Scholar 

  • Forst S, Dowds B, Boemare N et al (1997) Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51:47–72

    Article  CAS  PubMed  Google Scholar 

  • Fuchs SW, Proschak A, Jaskolla TW et al (2011) Structure elucidation and biosynthesis of lysine-rich cyclic peptides in Xenorhabdus nematophila. Org Biomol Chem 9:3130–3132

    Article  CAS  PubMed  Google Scholar 

  • Goh EB, Yim G, Tsui W et al (2002) Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci U S A 99:17025–17030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodrich-Blair H, Clarke DJ (2007) Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64:260–268

    Article  CAS  PubMed  Google Scholar 

  • Gouge DH, Snyder JL (2006) Temporal association of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) and bacteria. J Invertebr Pathol 91:147–157

    Article  PubMed  Google Scholar 

  • Gualtieri M, Aumelas A, Thaler JO (2009) Identification of a new antimicrobial lysine-rich cyclolipopeptide family from Xenorhabdus nematophila. J Antibiot (Tokyo) 62:295–302

    Article  CAS  Google Scholar 

  • Hibbing ME, Fuqua C, Parsek MR et al (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang J, Park Y, Kim Y et al (2013) An entomopathogenic bacterium, Xenorhabdus nematophila, suppresses expression of antimicrobial peptides controlled by Toll and Imd pathways by blocking eicosanoid biosynthesis. Arch Insect Biochem Physiol 83:151–169

    Article  CAS  PubMed  Google Scholar 

  • Ishii S-I, Nishi Y, Egami F (1965) The fine structure of a pyocin. J Mol Biol 13:428–431

    Article  CAS  PubMed  Google Scholar 

  • Itoh Y, Izaki K, Takahashi H (1978) Purification and characterization of a bacteriocin from Erwinia carotovora. J Gen Appl Microbiol 24:27–39

    Article  CAS  Google Scholar 

  • Jabrane A, Sabri A, Compere P et al (2002) Characterization of serracin P, a phage-tail-like bacteriocin, and its activity against Erwinia amylovora, the fire blight pathogen. Appl Environ Microbiol 68:5704–5710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji D, Yi Y, Kang GH et al (2004) Identification of an antibacterial compound, benzylideneacetone, from Xenorhabdus nematophila against major plant-pathogenic bacteria. FEMS Microbiol Lett 239:241–248

    Article  CAS  PubMed  Google Scholar 

  • Jubelin G, Pages S, Lanois A et al (2011) Studies of the dynamic expression of the Xenorhabdus FliAZ regulon reveal atypical iron-dependent regulation of the flagellin and haemolysin genes during insect infection. Environ Microbiol 13:1271–1284

    Article  CAS  PubMed  Google Scholar 

  • Kegler C, Nollmann FI, Ahrendt T et al (2014) Rapid determination of the amino acid configuration of xenotetrapeptide. Chembiochem 15:826–828

    Article  CAS  PubMed  Google Scholar 

  • Koppenhoefer AM, Kaya HK (1996) Coexistence of two steinernematid nematode species (Rhabditida:Steinernematidae) in the presence of two host species. Appl Soil Ecol 4:221–230

    Article  Google Scholar 

  • Krin E, Chakroun N, Turlin E et al (2006) Pleiotropic role of quorum-sensing autoinducer 2 in Photorhabdus luminescens. Appl Environ Microbiol 72:6439–6451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang G, Kalvelage T, Peters A et al (2008) Linear and cyclic peptides from the entomopathogenic bacterium Xenorhabdus nematophilus. J Nat Prod 71:1074–1077

    Article  CAS  PubMed  Google Scholar 

  • Lango-Scholey L, Brachmann AO, Bode HB et al (2013) The expression of stlA in Photorhabdus luminescens ss controlled by nutrient limitation. PLoS One 8, e82152

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee MM, Stock SP (2010) A multigene approach for assessing evolutionary relationships of Xenorhabdus spp. (gamma-Proteobacteria), the bacterial symbionts of entomopathogenic Steinernema nematodes. J Invertebr Pathol 104:67–74

    Article  CAS  PubMed  Google Scholar 

  • Li J, Chen G, Webster JM (1997) Nematophin, a novel antimicrobial substance produced by Xenorhabdus nematophilus (Enterobacteriaceae). Can J Microbiol 43:770–773

    Article  CAS  PubMed  Google Scholar 

  • Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367

    Article  PubMed  Google Scholar 

  • Maxwell PW, Chen G, Webster JM et al (1994) Stability and activities of antibiotics produced during infection of the insect Galleria mellonella by two isolates of Xenorhabdus nematophilus. Appl Environ Microbiol 60:715–721

    CAS  PubMed  PubMed Central  Google Scholar 

  • McInerney BV, Taylor WC, Lacey MJ et al (1991) Biologically active metabolites from Xenorhabdus spp., Part 2. Benzopyran-1-one derivatives with gastroprotective activity. J Nat Prod 54:785–795

    Article  CAS  PubMed  Google Scholar 

  • Mlot C (2009) Antibiotics in nature: beyond biological warfare. Science 324:1637–1639

    Article  CAS  PubMed  Google Scholar 

  • Moore AJ, Beazley WD, Bibby MC et al (1996) Antimicrobial activity of cecropins. J Antimicrob Chemother 37:1077–1089

    Article  CAS  PubMed  Google Scholar 

  • Morales-Soto N, Forst SA (2011) The xnp1 P2-like tail synthesis gene cluster encodes xenorhabdicin and is required for interspecies competition. J Bacteriol 193:3624–3632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morales-Soto N, Snyder H, Forst S (2009) Interspecies competition in a bacteria-nematode mutualism. In: White JF, Torres MS (eds) Defensive mutualism in microbial symbiosis. Taylor and Francis Group, LLC, Boca Raton, FL, pp 117–127

    Google Scholar 

  • Morales-Soto N, Gaudriault S, Ogier JC et al (2012) Comparative analysis of P2-type remnant prophage loci in Xenorhabdus bovienii and Xenorhabdus nematophila required for xenorhabdicin production. FEMS Microbiol Lett 333:69–76

    Article  CAS  PubMed  Google Scholar 

  • Park D, Forst S (2006) Co-regulation of motility, exoenzyme and antibiotic production by the EnvZ-OmpR-FlhDC-FliA pathway in Xenorhabdus nematophila. Mol Microbiol 61:1397–1412

    Article  CAS  PubMed  Google Scholar 

  • Park D, Ciezki K, Van der Hoeven R et al (2009) Genetic analysis of xenocoumacin antibiotic production in the mutualistic bacterium Xenorhabdus nematophila. Mol Microbiol 73:938–949

    Article  CAS  PubMed  Google Scholar 

  • Paul VJ, Frautschy S, Fenical W et al (1981) Antibiotics in microbial ecology, isolation and structure assignment of several new antibacterial compounds from the insect-symbiotic bacteria Xenorhabdus spp. J Chem Ecol 7:589–597

    Article  CAS  PubMed  Google Scholar 

  • Reimer D, Luxenburger E, Brachmann AO et al (2009) A new type of pyrrolidine biosynthesis is involved in the late steps of xenocoumacin production in Xenorhabdus nematophila. Chembiochem 10:1997–2001

    Article  CAS  PubMed  Google Scholar 

  • Reimer D, Pos KM, Thines M et al (2011) A natural prodrug activation mechanism in nonribosomal peptide synthesis. Nat Chem Biol 7:888–890

    Article  CAS  PubMed  Google Scholar 

  • Reimer D, Cowles KN, Proschak A et al (2013) Rhabdopeptides as insect-specific virulence factors from entomopathogenic bacteria. Chembiochem 14:1991–1997

    Article  CAS  PubMed  Google Scholar 

  • Reimer D, Nollman FI, Schultz K et al (2014) Xenortide biosynthesis by entomopathogenic Xenorhabdus nematophila. J Nat Prod 77(8):1976–1980

    Article  CAS  PubMed  Google Scholar 

  • Riaz K, Elmerich C, Moreira D et al (2008) A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ Microbiol 10:560–570

    Article  CAS  PubMed  Google Scholar 

  • Romero D, Traxler MF, Lopez D et al (2011) Antibiotics as signal molecules. Chem Rev 111:5492–5505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz S (2014) A new bacterial chemical signal: mapping the chemical space used for communication. Chembiochem 15:498–500

    Article  CAS  PubMed  Google Scholar 

  • Seipke RF, Barke J, Brearley C et al (2011) A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS One 6, e22028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo S, Lee S, Hong Y et al (2012) Phospholipase A2 inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl Environ Microbiol 78:3816–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sicard M, Brugirard-Ricaud K, Pages S et al (2004) Stages of infection during the tripartite interaction between Xenorhabdus nematophila, its nematode vector, and insect hosts. Appl Environ Microbiol 70:6473–6480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sicard M, Tabart J, Boemare NE et al (2005) Effect of phenotypic variation in Xenorhabdus nematophila on its mutualistic relationship with the entomopathogenic nematode Steinernema carpocapsae. Parasitology 131:687–694

    Article  CAS  PubMed  Google Scholar 

  • Sicard M, Hinsinger J, Le Brun N et al (2006) Interspecific competition between entomopathogenic nematodes (Steinernema) is modified by their bacterial symbionts (Xenorhabdus). BMC Evol Biol 6:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh J, Banerjee N (2008) Transcriptional analysis and functional characterization of a gene pair encoding iron-regulated xenocin and immunity proteins of Xenorhabdus nematophila. J Bacteriol 190:3877–3885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh P, Park D, Forst S et al (2013) Xenocin export by the flagellar type III pathway in Xenorhabdus nematophila. J Bacteriol 195:1400–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh S, Reese JM, Casanova-Torres ÁM et al (2014) Microbial population dynamics in the hemolymph of Manduca sexta infected with Xenorhabdus nematophila and the entomopathogenic nematode Steinernema carpocapsae. Appl Environ Microbiol 80:4277–4285

    Article  PubMed  PubMed Central  Google Scholar 

  • Snyder H, Stock SP, Kim SK et al (2007) New insights into the colonization and release processes of Xenorhabdus nematophila and the morphology and ultrastructure of the bacterial receptacle of its nematode host, Steinernema carpocapsae. Appl Environ Microbiol 73:5338–5346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somvanshi VS, Sloup RE, Crawford JM et al (2012) A single promoter inversion switches Photorhabdus between pathogenic and mutualistic states. Science 337:88–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song CJ, Seo S, Shrestha S et al (2011) Bacterial metabolites of an entomopathogenic bacterium, Xenorhabdus nematophila, inhibit a catalytic activity of phenoloxidase of the diamondback moth, Plutella xylostella. J Microbiol Biotechnol 21:317–322

    CAS  PubMed  Google Scholar 

  • Sun SC, Lindstrom I, Boman HG et al (1990) Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 250:1729–1732

    Article  CAS  PubMed  Google Scholar 

  • Sundar L, Chang FN (1993) Antimicrobial activity and biosynthesis of indole antibiotics produced by Xenorhabdus nematophilus. J Gen Microbiol 139:3139–3148

    Article  CAS  PubMed  Google Scholar 

  • Tani TH, Khodursky A, Blumenthal RM et al (2002) Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis. Proc Natl Acad Sci U S A 99:13471–13476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thaler JO, Baghdiguian S, Boemare N (1995) Purification and characterization of xenorhabdicin, a phage tail-like bacteriocin, from the lysogenic strain F1 of Xenorhabdus nematophilus. Appl Environ Microbiol 61:2049–2052

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uratani Y (1982) Dansyl chloride labeling of Pseudomonas aeruginosa treated with pyocin R1: change in permeability of the cell envelope. J Bacteriol 149:523–528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uratani Y, Hoshino T (1984) Pyocin R1 inhibits active transport in Pseudomonas aeruginosa and depolarizes membrane potential. J Bacteriol 157:632–636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Volgyi A, Fodor A, Szentirmai A et al (1998) Phase Variation in Xenorhabdus nematophilus. Appl Environ Microbiol 64:1188–1193

    CAS  PubMed  PubMed Central  Google Scholar 

  • Volgyi A, Fodor A, Forst S (2000) Inactivation of a novel gene produces a phenotypic variant cell and affects the symbiotic behavior of Xenorhabdus nematophilus. Appl Environ Microbiol 66:1622–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams JS, Thomas M, Clarke DJ (2005) The gene stlA encodes a phenylalanine ammonia-lyase that is involved in the production of a stilbene antibiotic in Photorhabdus luminescens TT01. Microbiology 151:2543–2550

    Article  CAS  PubMed  Google Scholar 

  • Yim G, Wang HH, Davies J (2006) The truth about antibiotics. Int J Med Microbiol 296:163–170

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Biological Sciences, University of Wisconsin, Milwaukee, WI, 53201, USA

    Swati Singh & Steven Forst

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  1. Swati Singh
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  2. Steven Forst
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Correspondence to Steven Forst .

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    Christon J. Hurst

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Singh, S., Forst, S. (2016). Antimicrobials and the Natural Biology of a Bacterial-Nematode Symbiosis. In: Hurst, C. (eds) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-28068-4_5

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