Candidatus Streptomyces philanthi-is a monophyletic clade of formerly uncultured bacterial symbionts in solitary digger wasps of the genera Philanthus, Philanthinus and Trachypus (Hymenoptera, Crabronidae). These bacteria grow in female-specific antennal reservoirs and -after transmission to the cocoon -produce antibiotics protecting the host larvae from fungal infection. However, the symbionts-refractoriness to cultivation has thus far hampered detailed in vitro studies on their physiology and on the evolutionary changes in metabolic versatility in response to the host environment. Results Here we isolated in axenic culture 22 -em class="a-plus-plus">Streptomyces philanthi-biovars from different host species. Sequencing of gyrB revealed no heterogeneity among isolates within host individuals, suggesting low levels of (micro)diversity or even clonality of the symbionts in individual beewolf antennae. Surprisingly, however, isolates from different host species differed strongly in their physiology. All biovars from the Eurasian/African Philanthus and the South American Trachypus host species had high nutritional demands and were susceptible to most antibiotics tested, suggesting a tight association with the hosts. By contrast, biovars isolated from the genus Philanthinus and the monophyletic North American Philanthus clade were metabolically versatile and showed broad antibiotic resistance. Concordantly, recent horizontal symbiont transfer events -reflected in different symbiont strains infecting the same host species -have been described only among North American Philanthus species, altogether indicative of facultative symbionts potentially capable of a free-living lifestyle. Phylogenetic analyses reveal a strong correlation between symbiont metabolic versatility and host phylogeny, suggesting that the host environment differentially affects the symbionts-evolutionary fate. Although opportunistic bacteria were occasionally isolated from the antennae of different host species, only filamentous Actinobacteria (genera Streptomyces, Amycolatopsis and Nocardia) could replace -em class="a-plus-plus">S. philanthi-in the antennal gland reservoirs. Conclusion Our results indicate that closely related bacteria from a monophyletic clade of symbionts can experience very different evolutionary trajectories in response to the symbiotic lifestyle, which is reflected in different degrees of metabolic versatility and host-dependency. We propose that the host-provided environment could be an important factor in shaping the degenerative metabolic evolution in the symbionts and deciding whether they evolve into obligate symbionts or remain facultative and capable of a host-independent lifestyle." />
Cultivation reveals physiological diversity among defensive -em class="a-plus-plus">Streptomyces philanthi-/em> symbionts of beewolf digger wasps (Hymenoptera, Crabronidae)
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  • 作者:Taras Y Nechitaylo ; Martin Westermann ; Martin Kaltenpoth
  • 关键词:Streptomyces ; Physiology ; Symbiosis ; Mutualism ; Co ; evolution ; Beewolf ; Digger wasp
  • 刊名:BMC Microbiology
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:14
  • 期:1
  • 全文大小:3,299 KB
  • 参考文献:1. Moran, NA (2006) Symbiosis. Curr Biol 16: pp. R866-R871 CrossRef
    2. Feldhaar, H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36: pp. 533-543 CrossRef
    3. Pontes, MH, Dale, C (2006) Culture and manipulation of insect facultative symbionts. Trends Microbiol 14: pp. 406-412 CrossRef
    4. Kim, JK, Won, YJ, Nikoh, N, Nakayama, H, Han, SH, Kikuchi, Y, Rhee, YH, Park, HY, Kwon, JY, Kurokawa, K, Dohmae, N, Fukatsu, T, Lee, BL (2013) Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis. Proc Natl Acad Sci U S A 110: pp. E2381-E2389 CrossRef
    5. Kim JK, Lee HJ, Kikuchi Y, Kitagawa W, Nikoh N, Fukatsu T, Lee BL: Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the stinkbug gut. / Appl Environ Microbiol 2013, 79:4879-886.
    6. Dale, C, Beeton, M, Harbison, C, Jones, T, Pontes, M (2006) Isolation, pure culture, and characterization of “Candidatus Arsenophonus arthropodicus- an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72: pp. 2997-3004 CrossRef
    7. Dulla, GFJ, Go, RA, Stahl, DA, Davidson, SK (2012) Verminephrobacter eiseniae type IV pili and flagella are required to colonize earthworm nephridia. ISME J 6: pp. 1166-1175 CrossRef
    8. Bourtzis, K, Miller, TA (2004) Insect Symbiosis. Taylor & Francis, Boca Raton, USA
    9. Brownlie, JC, Johnson, KN (2009) Symbiont-mediated protection in insect hosts. Trends Microbiol 17: pp. 348-354 CrossRef
    10. Kaltenpoth, M, Engl, T (2013) Defensive microbial symbionts in Hymenoptera. Functional Ecol 28: pp. 315-327 CrossRef
    11. Seipke, RF, Kaltenpoth, M, Hutchings, MI (2011) Streptomyces as symbionts: an emerging and widespread theme?. FEMS Microbiol Rev 36: pp. 862-876 CrossRef
    12. Kaltenpoth, M (2009) Actinobacteria as mutualists: general healthcare for insects?. Trends Microbiol 17: pp. 529-535 CrossRef
    13. Currie, CR, Scott, JA, Summerbell, RC, Malloch, D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: pp. 701-704 CrossRef
    14. Haeder S, Wirth R, Herz H, Spiteller D: Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis . / Proc Natl Acad Sci U S A 2009, 106:4742-746.
    15. Barke J, Seipke RF, Gruschow S, Heavens D, Drou N, Bibb MJ, Goss RJ, Yu DW, Hutchings MI: A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus . / BMC Biol 2010, 8:109.
    16. Scott, JJ, Oh, DC, Yuceer, MC, Klepzig, KD, Clardy, J, Currie, CR (2008) Bacterial protection of beetle-fungus mutualism. Science 322: pp. 63 CrossRef
    17. Kaltenpoth, M, Gottler, W, Herzner, G, Strohm, E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15: pp. 475-479
  • 刊物主题:Microbiology; Biological Microscopy; Fungus Genetics; Parasitology; Virology; Life Sciences, general;
  • 出版者:BioMed Central
  • ISSN:1471-2180
文摘
Background -em class="a-plus-plus">Candidatus Streptomyces philanthi-is a monophyletic clade of formerly uncultured bacterial symbionts in solitary digger wasps of the genera Philanthus, Philanthinus and Trachypus (Hymenoptera, Crabronidae). These bacteria grow in female-specific antennal reservoirs and -after transmission to the cocoon -produce antibiotics protecting the host larvae from fungal infection. However, the symbionts-refractoriness to cultivation has thus far hampered detailed in vitro studies on their physiology and on the evolutionary changes in metabolic versatility in response to the host environment. Results Here we isolated in axenic culture 22 -em class="a-plus-plus">Streptomyces philanthi-biovars from different host species. Sequencing of gyrB revealed no heterogeneity among isolates within host individuals, suggesting low levels of (micro)diversity or even clonality of the symbionts in individual beewolf antennae. Surprisingly, however, isolates from different host species differed strongly in their physiology. All biovars from the Eurasian/African Philanthus and the South American Trachypus host species had high nutritional demands and were susceptible to most antibiotics tested, suggesting a tight association with the hosts. By contrast, biovars isolated from the genus Philanthinus and the monophyletic North American Philanthus clade were metabolically versatile and showed broad antibiotic resistance. Concordantly, recent horizontal symbiont transfer events -reflected in different symbiont strains infecting the same host species -have been described only among North American Philanthus species, altogether indicative of facultative symbionts potentially capable of a free-living lifestyle. Phylogenetic analyses reveal a strong correlation between symbiont metabolic versatility and host phylogeny, suggesting that the host environment differentially affects the symbionts-evolutionary fate. Although opportunistic bacteria were occasionally isolated from the antennae of different host species, only filamentous Actinobacteria (genera Streptomyces, Amycolatopsis and Nocardia) could replace -em class="a-plus-plus">S. philanthi-in the antennal gland reservoirs. Conclusion Our results indicate that closely related bacteria from a monophyletic clade of symbionts can experience very different evolutionary trajectories in response to the symbiotic lifestyle, which is reflected in different degrees of metabolic versatility and host-dependency. We propose that the host-provided environment could be an important factor in shaping the degenerative metabolic evolution in the symbionts and deciding whether they evolve into obligate symbionts or remain facultative and capable of a host-independent lifestyle.

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