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The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus

BACKGROUND: Pine wilt disease (PWD) is a worldwide threat to pine forests, and is caused by the pine wood nematode (PWN) Bursaphelenchus xylophilus. Bacteria are known to be associated with PWN and may have an important role in PWD. Serratia sp. LCN16 is a PWN-associated bacterium, highly resistant...

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Autores principales: Vicente, Claudia S. L., Nascimento, Francisco X., Ikuyo, Yoriko, Cock, Peter J. A., Mota, Manuel, Hasegawa, Koichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4841953/
https://www.ncbi.nlm.nih.gov/pubmed/27108223
http://dx.doi.org/10.1186/s12864-016-2626-1
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author Vicente, Claudia S. L.
Nascimento, Francisco X.
Ikuyo, Yoriko
Cock, Peter J. A.
Mota, Manuel
Hasegawa, Koichi
author_facet Vicente, Claudia S. L.
Nascimento, Francisco X.
Ikuyo, Yoriko
Cock, Peter J. A.
Mota, Manuel
Hasegawa, Koichi
author_sort Vicente, Claudia S. L.
collection PubMed
description BACKGROUND: Pine wilt disease (PWD) is a worldwide threat to pine forests, and is caused by the pine wood nematode (PWN) Bursaphelenchus xylophilus. Bacteria are known to be associated with PWN and may have an important role in PWD. Serratia sp. LCN16 is a PWN-associated bacterium, highly resistant to oxidative stress in vitro, and which beneficially contributes to the PWN survival under these conditions. Oxidative stress is generated as a part of the basal defense mechanism used by plants to combat pathogenic invasion. Here, we studied the biology of Serratia sp. LCN16 through genome analyses, and further investigated, using reverse genetics, the role of two genes directly involved in the neutralization of H(2)O(2), namely the H(2)O(2) transcriptional factor oxyR; and the H(2)O(2)-targeting enzyme, catalase katA. RESULTS: Serratia sp. LCN16 is phylogenetically most closely related to the phytosphere group of Serratia, which includes S. proteamaculans, S. grimessi and S. liquefaciens. Likewise, Serratia sp. LCN16 shares many features with endophytes (plant-associated bacteria), such as genes coding for plant polymer degrading enzymes, iron uptake/transport, siderophore and phytohormone synthesis, aromatic compound degradation and detoxification enzymes. OxyR and KatA are directly involved in the high tolerance to H(2)O(2) of Serratia sp. LCN16. Under oxidative stress, Serratia sp. LCN16 expresses katA independently of OxyR in contrast with katG which is under positive regulation of OxyR. Serratia sp. LCN16 mutants for oxyR (oxyR::int(614)) and katA (katA::int(808)) were sensitive to H(2)O(2) in relation with wild-type, and both failed to protect the PWN from H(2)O(2)-stress exposure. Moreover, both mutants showed different phenotypes in terms of biofilm production and swimming/swarming behaviors. CONCLUSIONS: This study provides new insights into the biology of PWN-associated bacteria Serratia sp. LCN16 and its extreme resistance to oxidative stress conditions, encouraging further research on the potential role of this bacterium in interaction with PWN in planta environment. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2626-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-48419532016-04-24 The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus Vicente, Claudia S. L. Nascimento, Francisco X. Ikuyo, Yoriko Cock, Peter J. A. Mota, Manuel Hasegawa, Koichi BMC Genomics Research Article BACKGROUND: Pine wilt disease (PWD) is a worldwide threat to pine forests, and is caused by the pine wood nematode (PWN) Bursaphelenchus xylophilus. Bacteria are known to be associated with PWN and may have an important role in PWD. Serratia sp. LCN16 is a PWN-associated bacterium, highly resistant to oxidative stress in vitro, and which beneficially contributes to the PWN survival under these conditions. Oxidative stress is generated as a part of the basal defense mechanism used by plants to combat pathogenic invasion. Here, we studied the biology of Serratia sp. LCN16 through genome analyses, and further investigated, using reverse genetics, the role of two genes directly involved in the neutralization of H(2)O(2), namely the H(2)O(2) transcriptional factor oxyR; and the H(2)O(2)-targeting enzyme, catalase katA. RESULTS: Serratia sp. LCN16 is phylogenetically most closely related to the phytosphere group of Serratia, which includes S. proteamaculans, S. grimessi and S. liquefaciens. Likewise, Serratia sp. LCN16 shares many features with endophytes (plant-associated bacteria), such as genes coding for plant polymer degrading enzymes, iron uptake/transport, siderophore and phytohormone synthesis, aromatic compound degradation and detoxification enzymes. OxyR and KatA are directly involved in the high tolerance to H(2)O(2) of Serratia sp. LCN16. Under oxidative stress, Serratia sp. LCN16 expresses katA independently of OxyR in contrast with katG which is under positive regulation of OxyR. Serratia sp. LCN16 mutants for oxyR (oxyR::int(614)) and katA (katA::int(808)) were sensitive to H(2)O(2) in relation with wild-type, and both failed to protect the PWN from H(2)O(2)-stress exposure. Moreover, both mutants showed different phenotypes in terms of biofilm production and swimming/swarming behaviors. CONCLUSIONS: This study provides new insights into the biology of PWN-associated bacteria Serratia sp. LCN16 and its extreme resistance to oxidative stress conditions, encouraging further research on the potential role of this bacterium in interaction with PWN in planta environment. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2626-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-04-23 /pmc/articles/PMC4841953/ /pubmed/27108223 http://dx.doi.org/10.1186/s12864-016-2626-1 Text en © Vicente et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Vicente, Claudia S. L.
Nascimento, Francisco X.
Ikuyo, Yoriko
Cock, Peter J. A.
Mota, Manuel
Hasegawa, Koichi
The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title_full The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title_fullStr The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title_full_unstemmed The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title_short The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus
title_sort genome and genetics of a high oxidative stress tolerant serratia sp. lcn16 isolated from the plant parasitic nematode bursaphelenchus xylophilus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4841953/
https://www.ncbi.nlm.nih.gov/pubmed/27108223
http://dx.doi.org/10.1186/s12864-016-2626-1
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