Microbiome and infectivity studies reveal complex polyspecies tree disease in Acute Oak Decline

Sandra Denman, James Doonan, Emma Ransom-Jones, Martin Broberg, Sarah Plummer, Susan Kirk, Kelly Scarlett, Andrew R. Griffiths, Maciej Kaczmarek, Jack Forster, Andrew Peace, Peter N. Golyshin, Francis Hassard, Nathan Brown, John G. Kenny, James E. McDonald

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Decline-diseases are complex and becoming increasingly problematic to tree health globally. Acute Oak Decline (AOD) is characterized by necrotic stem lesions and galleries of the bark-boring beetle, Agrilus biguttatus, and represents a serious threat to oak. Although multiple novel bacterial species and Agrilus galleries are associated with AOD lesions, the causative agent(s) are unknown. The AOD pathosystem therefore provides an ideal model for a systems-based research approach to address our hypothesis that AOD lesions are caused by a polymicrobial complex. Here we show that three bacterial species, Brenneria goodwinii, Gibbsiella quercinecans and Rahnella victoriana, are consistently abundant in the lesion microbiome and possess virulence genes used by canonical phytopathogens that are expressed in AOD lesions. Individual and polyspecies inoculations on oak logs and trees demonstrated that B. goodwinii and G. quercinecans cause tissue necrosis and, in combination with A. biguttatus, produce the diagnostic symptoms of AOD. We have proved a polybacterial cause of AOD lesions, providing new insights into polymicrobial interactions and tree disease. This work presents a novel conceptual and methodological template for adapting Koch's postulates to address the role of microbial communities in disease.
Original languageEnglish
Pages (from-to)386-399
Number of pages14
JournalISME Journal
Volume12
Early online date13 Oct 2017
DOIs
Publication statusPublished - Feb 2018
Externally publishedYes

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tree diseases
infectivity
Microbiota
Acute Disease
lesions (plant)
Quercus
pathogenicity
lesion
Rahnella
Beetles
Agrilus
Virulence
Necrosis
Brenneria
Health
Research
wood logs
Genes
microbiome
oak

Cite this

Denman, Sandra ; Doonan, James ; Ransom-Jones, Emma ; Broberg, Martin ; Plummer, Sarah ; Kirk, Susan ; Scarlett, Kelly ; Griffiths, Andrew R. ; Kaczmarek, Maciej ; Forster, Jack ; Peace, Andrew ; Golyshin, Peter N. ; Hassard, Francis ; Brown, Nathan ; Kenny, John G. ; McDonald, James E. / Microbiome and infectivity studies reveal complex polyspecies tree disease in Acute Oak Decline. In: ISME Journal. 2018 ; Vol. 12. pp. 386-399.
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abstract = "Decline-diseases are complex and becoming increasingly problematic to tree health globally. Acute Oak Decline (AOD) is characterized by necrotic stem lesions and galleries of the bark-boring beetle, Agrilus biguttatus, and represents a serious threat to oak. Although multiple novel bacterial species and Agrilus galleries are associated with AOD lesions, the causative agent(s) are unknown. The AOD pathosystem therefore provides an ideal model for a systems-based research approach to address our hypothesis that AOD lesions are caused by a polymicrobial complex. Here we show that three bacterial species, Brenneria goodwinii, Gibbsiella quercinecans and Rahnella victoriana, are consistently abundant in the lesion microbiome and possess virulence genes used by canonical phytopathogens that are expressed in AOD lesions. Individual and polyspecies inoculations on oak logs and trees demonstrated that B. goodwinii and G. quercinecans cause tissue necrosis and, in combination with A. biguttatus, produce the diagnostic symptoms of AOD. We have proved a polybacterial cause of AOD lesions, providing new insights into polymicrobial interactions and tree disease. This work presents a novel conceptual and methodological template for adapting Koch's postulates to address the role of microbial communities in disease.",
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Denman, S, Doonan, J, Ransom-Jones, E, Broberg, M, Plummer, S, Kirk, S, Scarlett, K, Griffiths, AR, Kaczmarek, M, Forster, J, Peace, A, Golyshin, PN, Hassard, F, Brown, N, Kenny, JG & McDonald, JE 2018, 'Microbiome and infectivity studies reveal complex polyspecies tree disease in Acute Oak Decline', ISME Journal, vol. 12, pp. 386-399. https://doi.org/10.1038/ismej.2017.170

Microbiome and infectivity studies reveal complex polyspecies tree disease in Acute Oak Decline. / Denman, Sandra; Doonan, James; Ransom-Jones, Emma; Broberg, Martin; Plummer, Sarah; Kirk, Susan; Scarlett, Kelly; Griffiths, Andrew R.; Kaczmarek, Maciej; Forster, Jack; Peace, Andrew; Golyshin, Peter N.; Hassard, Francis; Brown, Nathan; Kenny, John G.; McDonald, James E.

In: ISME Journal, Vol. 12, 02.2018, p. 386-399.

Research output: Contribution to journalArticle

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AU - Forster, Jack

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AU - McDonald, James E.

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N2 - Decline-diseases are complex and becoming increasingly problematic to tree health globally. Acute Oak Decline (AOD) is characterized by necrotic stem lesions and galleries of the bark-boring beetle, Agrilus biguttatus, and represents a serious threat to oak. Although multiple novel bacterial species and Agrilus galleries are associated with AOD lesions, the causative agent(s) are unknown. The AOD pathosystem therefore provides an ideal model for a systems-based research approach to address our hypothesis that AOD lesions are caused by a polymicrobial complex. Here we show that three bacterial species, Brenneria goodwinii, Gibbsiella quercinecans and Rahnella victoriana, are consistently abundant in the lesion microbiome and possess virulence genes used by canonical phytopathogens that are expressed in AOD lesions. Individual and polyspecies inoculations on oak logs and trees demonstrated that B. goodwinii and G. quercinecans cause tissue necrosis and, in combination with A. biguttatus, produce the diagnostic symptoms of AOD. We have proved a polybacterial cause of AOD lesions, providing new insights into polymicrobial interactions and tree disease. This work presents a novel conceptual and methodological template for adapting Koch's postulates to address the role of microbial communities in disease.

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