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Letter to the Editor | Applied and Environmental Science

Precedence for the Role of Indole with Pathogens

Thomas K. Wood, Jintae Lee
Arturo Casadevall, Editor
Thomas K. Wood
aDepartment of Chemical Engineering, Pennsylvania State University, University Park, Pennsylvania, USA
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Jintae Lee
bSchool of Chemical Engineering, Yeungnam University, Gyeongsan, Gyeongbuk, South Korea
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Arturo Casadevall
Johns Hopkins Bloomberg School of Public Health
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DOI: 10.1128/mBio.01599-19
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LETTER

Continuing the trend of impressive results demonstrating the importance of indole as an interspecies (1, 2) and interkingdom (3) signal that reduces pathogenicity (1), Kumar and Sperandio recently reported that indole represses the expression of virulence genes of the gastrointestinal tract pathogens enterohemorrhagic Escherichia coli (EHEC) and Citrobacter rodentium (4). However, we wish to point out several omissions from their paper.

With regard to the mechanism reported by Kumar and Sperandio for sensing indole through the histidine kinase sensor CpxA of EHEC (4), it is important to note that this was discovered 14 years earlier for E. coli by Hirakawa et al. (5). These researchers found that indole sensing in commensal E. coli requires the BaeSR and CpxAR two-component systems. Unfortunately, this contribution was not cited by Kumar and Sperandio (4).

Additional important omissions by Kumar and Sperandio (4) include that it is already established that indole reduces EHEC virulence, in that we showed 12 years earlier that indole repels EHEC (negative chemotaxis), reduces EHEC biofilm formation (a virulence trait), reduces EHEC motility, and reduces EHEC attachment to HeLa cells (a virulence trait) (6). Indole has also been shown to attenuate the pathogenicity of Staphylococcus aureus (7). Furthermore, indole has been shown previously to act as a true signal for E. coli (8), and it has been argued by us that indole is likely hydroxylated by oxygenases to become an even more potent signal in the gastrointestinal tract (8). Since commensal E. coli produces so much indole in the gastrointestinal tract, we have speculated that indole is the likely archetype for human hormones (2). Unfortunately, these references were not cited.

Furthermore, Kumar and Sperandio also failed to indicate that indole has been shown to reduce the virulence of Pseudomonas aeruginosa, another gastrointestinal tract pathogen, by decreasing its Pseudomonas quinolone signal (PQS), pyocyanin, rhamnolipid, and pyoverdine production (1). In addition, indole has been shown to increase the competitiveness of commensal E. coli with P. aeruginosa by inhibiting its quorum sensing (9). These references are also missing.

Kumar and Sperandio concluded that manipulation of indole concentrations in the gastrointestinal tract by pre- or probiotics that produce indole can limit the virulence of enteric pathogens (4); however, the use of indole as an antivirulence compound was suggested before by our group (1, 10), and indole was used successfully to reduce the virulence of P. aeruginosa in guinea pigs (1). Hence, Kumar and Sperandio are not the first to show that indole reduces EHEC pathogenicity, not the first to indicate that indole is sensed via CpxAR, and not the first to show the importance of indole with non-E. coli strains (both pathogens and nonpathogens).

Lastly, it is worth noting that since indole reduces persistence (11, 12), it may be used by commensal E. coli to kill its dormant competitors (13). In a less belligerent role, indole is also used to keep pathogens asleep without affecting their growth (as it does for P. aeruginosa) to give commensal E. coli an advantage as it first wakes and forages for food (14).

FOOTNOTES

    • Published 30 July 2019
  • For the author reply, see https://doi.org/10.1128/mBio.01787-19.

  • Copyright © 2019 Wood and Lee.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

REFERENCES

  1. 1.↵
    1. Lee J,
    2. Attila C,
    3. Cirillo SLG,
    4. Cirillo JD,
    5. Wood TK
    . 2009. Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2:75–90. doi:10.1111/j.1751-7915.2008.00061.x.
    OpenUrlCrossRefPubMed
  2. 2.↵
    1. Lee J,
    2. Jayaraman A,
    3. Wood TK
    . 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7:42. doi:10.1186/1471-2180-7-42.
    OpenUrlCrossRefPubMed
  3. 3.↵
    1. Bansal T,
    2. Alaniz RC,
    3. Wood TK,
    4. Jayaraman A
    . 2010. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci U S A 107:228–233. doi:10.1073/pnas.0906112107.
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    1. Kumar A,
    2. Sperandio V
    . 2019. Indole signaling at the host-microbiota-pathogen interface. mBio 10:e01031-19. doi:10.1128/mBio.01031-19.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Hirakawa H,
    2. Inazumi Y,
    3. Masaki T,
    4. Hirata T,
    5. Yamaguchi A
    . 2004. Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126. doi:10.1111/j.1365-2958.2004.04449.x.
    OpenUrlCrossRef
  6. 6.↵
    1. Bansal T,
    2. Englert D,
    3. Lee J,
    4. Hegde M,
    5. Wood TK,
    6. Jayaraman A
    . 2007. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75:4597–4607. doi:10.1128/IAI.00630-07.
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    1. Lee J-H,
    2. Cho HS,
    3. Kim Y-G,
    4. Kim J-A,
    5. Banskota S,
    6. Cho MH,
    7. Lee J
    . 2013. Indole and 7-benzyloxyindole attenuate the virulence of Staphylococcus aureus. Appl Microbiol Biotechnol 97:4543. doi:10.1007/s00253-012-4674-z.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Lee J,
    2. Bansal T,
    3. Jayaraman A,
    4. Bentley WE,
    5. Wood TK
    . 2007. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 73:4100–4109. doi:10.1128/AEM.00360-07.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    1. Chu W,
    2. Zere TR,
    3. Weber MM,
    4. Wood TK,
    5. Whiteley M,
    6. Hidalgo-Romano B,
    7. Valenzuela E,
    8. McLean R
    . 2012. Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl Environ Microbiol 78:411–419. doi:10.1128/AEM.06396-11.
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    1. Lee J-H,
    2. Wood TK,
    3. Lee J
    . 2015. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23:707–718. doi:10.1016/j.tim.2015.08.001.
    OpenUrlCrossRefPubMed
  11. 11.↵
    1. Hu Y,
    2. Kwan BW,
    3. Osbourne DO,
    4. Benedik MJ,
    5. Wood TK
    . 2015. Toxin YafQ increases persister cell formation by reducing indole signalling. Environ Microbiol 17:1275–1285. doi:10.1111/1462-2920.12567.
    OpenUrlCrossRef
  12. 12.↵
    1. Kwan BW,
    2. Osbourne DO,
    3. Hu Y,
    4. Benedik MJ,
    5. Wood TK
    . 2015. Phosphodiesterase DosP increases persistence by reducing cAMP which reduces the signal indole. Biotechnol Bioeng 112:588–600. doi:10.1002/bit.25456.
    OpenUrlCrossRef
  13. 13.↵
    1. Lee J-H,
    2. Kim Y-G,
    3. Gwon G,
    4. Wood TK,
    5. Lee J
    . 2016. Halogenated indoles eradicate bacterial persister cells and biofilms. AMB Express 6:123. doi:10.1186/s13568-016-0297-6.
    OpenUrlCrossRef
  14. 14.↵
    1. Zhang W,
    2. Yamasaki R,
    3. Wood TK
    . 2019. Interkingdom signal indole inhibits Pseudomonas aeruginosa persister cell waking. bioRXiv doi:10.1101/674978.
    OpenUrlAbstract/FREE Full Text
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Precedence for the Role of Indole with Pathogens
Thomas K. Wood, Jintae Lee
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Precedence for the Role of Indole with Pathogens
Thomas K. Wood, Jintae Lee
mBio Jul 2019, 10 (4) e01599-19; DOI: 10.1128/mBio.01599-19
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KEYWORDS

environmental microbiology
gastrointestinal infection
indole

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