Molecular mechanisms underlying the close association between soil Burkholderia and fungi

Abstract

Bacterial species belonging to the genus Burkholderia have been repeatedly reported to be associated with fungi but the extent and specificity of these associations in soils remain undetermined. To assess whether associations between Burkholderia and fungi are widespread in soils, we performed a co-occurrence analysis in an intercontinental soil sample collection. This revealed that Burkholderia significantly co-occurred with a wide range of fungi. To analyse the molecular basis of the interaction, we selected two model fungi frequently co-occurring with Burkholderia, Alternaria alternata and Fusarium solani, and analysed the proteome changes caused by cultivation with either fungus in the widespread soil inhabitant B. glathei, whose genome we sequenced. Co-cultivation with both fungi led to very similar changes in the B. glathei proteome. Our results indicate that B. glathei significantly benefits from the interaction, which is exemplified by a lower abundance of several starvation factors that were highly expressed in pure culture. However, co-cultivation also gave rise to stress factors, as indicated by the increased expression of multidrug efflux pumps and proteins involved in oxidative stress response. Our data suggest that the ability of Burkholderia to establish a close association with fungi mainly lies in the capacities to utilize fungalsecreted metabolites and to overcome fungal defense mechanisms. This work indicates that beneficial interactions with fungi might contribute to the survival strategy of Burkholderia species in environments with sub-optimal conditions, including acidic soils.

The ecological role of volatile mediated interactions belowground

“…in the presence of F. culmorum indicating that additional nitrogen was provided by the fungal hyphae. In contrast, the up-regulation of bacterial genes related to uptake of alternative phosphate sources such as glycerol-3-phosphate (Stopnisek et al 2016) and genes related to phosphate starvation stress suggests that available phosphate was limited in fungal presence.…”

“…The occurrence of osmotic stress was also reported by Stopnisek et al (2016) for the interaction of Burkholderia strains with various fungi. While an association of Burkholderia to fungi was reported by several studies Uroz et al 2012;Nazir et al 2013;Stopnisek et al 2016), under the conditions used in our study, it seemed that the Burkholderia strain here was not able to colonize hyphae of F. culmorum. Genes involved in biofilm formation and defense mechanisms were down-regulated and the abundance was significantly decreased in in fungal presence.…”

“…Moreover, up-regulation of genes related to phospholipase C, Type VI secretion system and beta-lactamase by Collimonas pratensis as well as Dyella sp. in response to fungal presence further suggests that those bacteria acquired nutrients from living hyphae by disrupting the fungal membrane and defense system (Song et al 2015b;Journet & Cascales 2016 Leaking out nutrients such as trehalose, histidine, and carnitine potentially produced by F. culmorum (Table S6.14) might serve as carbon and nitrogen source for the bacteria (Wargo & Hogan 2009;Stopnisek et al 2016). Genes related to transport systems and degradation of those compounds were up-regulated by all bacteria, except Paenibacillus sp., in fungal presence.…”

“…Other than serving as potential carbon source, many aromatic compounds can have antimicrobial activity. Hence, the capacity to degrade those compounds might serve as protection for both, bacteria and fungus (Stopnisek et al 2016). …”

“…LRT = likelihood ratio test statistic. interaction is ectosymbiosis, where the bacterial partner is adhered to fungal hyphae Stopnisek et al 2016). …”