Brenneria goodwinii growth in vitro is improved by competitive interactions with other bacterial species associated with Acute Oak Decline

Carrie Brady; Mario Orsi; James M Doonan; Sandra Denman; Dawn Arnold

doi:10.1016/j.crmicr.2021.100102

Brenneria goodwinii growth in vitro is improved by competitive interactions with other bacterial species associated with Acute Oak Decline

Curr Res Microb Sci. 2021 Dec 20:3:100102. doi: 10.1016/j.crmicr.2021.100102. eCollection 2022.

Authors

Carrie Brady¹, Mario Orsi¹, James M Doonan², Sandra Denman³, Dawn Arnold^{1

4}

Affiliations

¹ Centre for Research in Bioscience, Faculty of Health and Life Sciences, University of the West of England, Coldharbour Lane, Bristol BS16 1QY, United Kingdom.
² Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958 Frederiksberg C, Denmark.
³ Centre for Forestry and Climate Change, Farnham, United Kingdom.
⁴ Harper Adams University, Newport, Shropshire TF10 8NB, United Kingdom.

Abstract

Brenneria goodwinii, Rahnella victoriana and Gibbsiella quercinecans are three bacterial species frequently isolated together from oak displaying symptoms of Acute Oak Decline (AOD), which include weeping patches on trunks. All three bacterial species play a role in lesion formation in the current episode of AOD in Britain, although B. goodwinii is the most dominant. The ongoing research into stem lesion formation characteristic of this polybacterial syndrome has been focussed primarily on the pathogenicity, identification and taxonomy of these bacteria. As all three species were newly classified within the past ten years, there are many unanswered questions regarding their ecology and interactions with each other. To determine the effect of bacterial interactions on fitness in vitro, we examined pairwise (diculture) and multispecies (triculture) interactions between B. goodwinii, R. victoriana and G. quercinecans in oak leaf media microcosms. Additionally, the effect of co-culturing on the evolution of these species was determined and the evolved B. goodwinii strains were examined further by whole genome sequencing. Our results indicate that B. goodwinii thrived in monoculture with significantly higher viable cell counts than the other two species. Additionally, B. goodwinii performed well in pairwise culture with mutually competitive interactions observed between B. goodwinii and R. victoriana, and between B. goodwinii and G. quercinecans. In the multispecies triculture, B. goodwinii and R. victoriana appeared to exhibit co-ordinated behaviour to outcompete G. quercinecans. After four weeks B. goodwinii grown in co-culture with the other two species developed greater evolved fitness than the strain grown in monoculture as reflected by the increased viable cell counts. The competitive interactions taking place between the threes species indicated evolving improved fitness of B. goodwinii in vitro, that gave it a growth advantage over both R. victoriana and G. quercinecans which showed no significant changes in fitness. Overall, B. goodwinii gains greater benefit in terms of fitness from in vitro competitive interaction with the other two species.

Keywords: AOD; Brenneria goodwinii; Competition; Fitness; Gibbsiella quercinecans; Interactions; Oak decline; Rahnella victoriana.