Literature DB >> 26116716

Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope.

Jiyeun Kate Kim1, Dae Woo Son1, Chan-Hee Kim1, Jae Hyun Cho1, Roberta Marchetti2, Alba Silipo2, Luisa Sturiale3, Ha Young Park1, Ye Rang Huh1, Hiroshi Nakayama4, Takema Fukatsu5, Antonio Molinaro2, Bok Luel Lee6.   

Abstract

The molecular characterization of symbionts is pivotal for understanding the cross-talk between symbionts and hosts. In addition to valuable knowledge obtained from symbiont genomic studies, the biochemical characterization of symbionts is important to fully understand symbiotic interactions. The bean bug (Riptortus pedestris) has been recognized as a useful experimental insect gut symbiosis model system because of its cultivatable Burkholderia symbionts. This system is greatly advantageous because it allows the acquisition of a large quantity of homogeneous symbionts from the host midgut. Using these naïve gut symbionts, it is possible to directly compare in vivo symbiotic cells with in vitro cultured cells using biochemical approaches. With the goal of understanding molecular changes that occur in Burkholderia cells as they adapt to the Riptortus gut environment, we first elucidated that symbiotic Burkholderia cells are highly susceptible to purified Riptortus antimicrobial peptides. In search of the mechanisms of the increased immunosusceptibility of symbionts, we found striking differences in cell envelope structures between cultured and symbiotic Burkholderia cells. The bacterial lipopolysaccharide O antigen was absent from symbiotic cells examined by gel electrophoretic and mass spectrometric analyses, and their membranes were more sensitive to detergent lysis. These changes in the cell envelope were responsible for the increased susceptibility of the Burkholderia symbionts to host innate immunity. Our results suggest that the symbiotic interactions between the Riptortus host and Burkholderia gut symbionts induce bacterial cell envelope changes to achieve successful gut symbiosis.
© 2015 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  Burkholderia; LPS; bean bug; gut symbionts; host defense; host-pathogen interaction; innate immunity; symbiosis

Mesh:

Substances:

Year:  2015        PMID: 26116716      PMCID: PMC4543662          DOI: 10.1074/jbc.M115.651158

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  40 in total

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Authors:  Mauricio H Pontes; Colin Dale
Journal:  Trends Microbiol       Date:  2006-07-27       Impact factor: 17.079

3.  Wolbachia density and virulence attenuation after transfer into a novel host.

Authors:  E A McGraw; D J Merritt; J N Droller; S L O'Neill
Journal:  Proc Natl Acad Sci U S A       Date:  2002-03-05       Impact factor: 11.205

4.  Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae).

Authors:  Yoshitomo Kikuchi; Xian-Ying Meng; Takema Fukatsu
Journal:  Appl Environ Microbiol       Date:  2005-07       Impact factor: 4.792

Review 5.  Microbe-associated molecular patterns in innate immunity: Extraction and chemical analysis of gram-negative bacterial lipopolysaccharides.

Authors:  Cristina De Castro; Michelangelo Parrilli; Otto Holst; Antonio Molinaro
Journal:  Methods Enzymol       Date:  2010       Impact factor: 1.600

6.  Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the Stinkbug Gut.

Authors:  Jiyeun Kate Kim; Ho Jin Lee; Yoshitomo Kikuchi; Wataru Kitagawa; Naruo Nikoh; Takema Fukatsu; Bok Luel Lee
Journal:  Appl Environ Microbiol       Date:  2013-06-07       Impact factor: 4.792

7.  Specific developmental window for establishment of an insect-microbe gut symbiosis.

Authors:  Yoshitomo Kikuchi; Takahiro Hosokawa; Takema Fukatsu
Journal:  Appl Environ Microbiol       Date:  2011-04-29       Impact factor: 4.792

8.  Specific midgut region controlling the symbiont population in an insect-microbe gut symbiotic association.

Authors:  Jiyeun Kate Kim; Na Hyang Kim; Ho Am Jang; Yoshitomo Kikuchi; Chan-Hee Kim; Takema Fukatsu; Bok Luel Lee
Journal:  Appl Environ Microbiol       Date:  2013-09-13       Impact factor: 4.792

Review 9.  Facultative symbionts in aphids and the horizontal transfer of ecologically important traits.

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Journal:  Annu Rev Entomol       Date:  2010       Impact factor: 19.686

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Authors:  Slade A Loutet; Miguel A Valvano
Journal:  Front Microbiol       Date:  2011-07-22       Impact factor: 5.640

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  15 in total

Review 1.  Bacterial strategies of resistance to antimicrobial peptides.

Authors:  Hwang-Soo Joo; Chih-Iung Fu; Michael Otto
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-05-26       Impact factor: 6.237

Review 2.  Perspectives on the evolutionary ecology of arthropod antimicrobial peptides.

Authors:  Jens Rolff; Paul Schmid-Hempel
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-05-26       Impact factor: 6.237

3.  Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture.

Authors:  Tsubasa Ohbayashi; Ryo Futahashi; Mia Terashima; Quentin Barrière; Florian Lamouche; Kazutaka Takeshita; Xian-Ying Meng; Yasuo Mitani; Teruo Sone; Shuji Shigenobu; Takema Fukatsu; Peter Mergaert; Yoshitomo Kikuchi
Journal:  ISME J       Date:  2019-02-11       Impact factor: 10.302

4.  Established Cotton Stainer Gut Bacterial Mutualists Evade Regulation by Host Antimicrobial Peptides.

Authors:  Thomas Ogao Onchuru; Martin Kaltenpoth
Journal:  Appl Environ Microbiol       Date:  2019-06-17       Impact factor: 4.792

5.  PhaR, a Negative Regulator of PhaP, Modulates the Colonization of a Burkholderia Gut Symbiont in the Midgut of the Host Insect, Riptortus pedestris.

Authors:  Seong Han Jang; Ho Am Jang; Junbeom Lee; Jong Uk Kim; Seung Ah Lee; Kyoung-Eun Park; Byung Hyun Kim; Yong Hun Jo; Bok Luel Lee
Journal:  Appl Environ Microbiol       Date:  2017-05-17       Impact factor: 4.792

6.  Identification and elucidation of proline-rich antimicrobial peptides with enhanced potency and delivery.

Authors:  Pin-Kuang Lai; Daniel T Tresnak; Benjamin J Hackel
Journal:  Biotechnol Bioeng       Date:  2019-07-21       Impact factor: 4.530

7.  Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body.

Authors:  Yoshiaki Kinosita; Yoshitomo Kikuchi; Nagisa Mikami; Daisuke Nakane; Takayuki Nishizaka
Journal:  ISME J       Date:  2017-12-21       Impact factor: 10.302

8.  The lipopolysaccharide core oligosaccharide of Burkholderia plays a critical role in maintaining a proper gut symbiosis with the bean bug Riptortus pedestris.

Authors:  Jiyeun Kate Kim; Ho Am Jang; Min Seon Kim; Jae Hyun Cho; Junbeom Lee; Flaviana Di Lorenzo; Luisa Sturiale; Alba Silipo; Antonio Molinaro; Bok Luel Lee
Journal:  J Biol Chem       Date:  2017-09-25       Impact factor: 5.157

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Authors:  Julia A Schwartzman; Edward G Ruby
Journal:  Trends Microbiol       Date:  2016-03-20       Impact factor: 17.079

10.  Immune tolerance to an intestine-adapted bacteria, Chryseobacterium sp., injected into the hemocoel of Protaetia brevitarsis seulensis.

Authors:  Jiae Lee; Sejung Hwang; Saeyoull Cho
Journal:  Sci Rep       Date:  2016-08-17       Impact factor: 4.379

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