Legacy effects of anaerobic soil disinfestation on soil bacterial community composition and production of pathogen-suppressing volatiles

Abstract

There is increasing evidence that microbial volatiles (VOCs) play an important role in natural suppression of soil-borne diseases, but little is known on the factors that influence production of suppressing VOCs. In the current study we examined whether a stress-induced change in soil microbial community composition would affect the production by soils of VOCs suppressing the plant-pathogenic oomycete Pythium. Using pyrosequencing of 16S ribosomal gene fragments we compared the composition of bacterial communities in sandy soils that had been exposed to anaerobic disinfestation (AD), a treatment used to kill harmful soil organisms, with the composition in untreated soils. Three months after the AD treatment had been finished, there was still a clear legacy effect of the former anaerobic stress on bacterial community composition with a strong increase in relative abundance of the phylum Bacteroidetes and a significant decrease of the phyla Acidobacteria, Planctomycetes, Nitrospirae, Chloroflexi, and Chlorobi. This change in bacterial community composition coincided with loss of production of Pythium suppressing soil volatiles (VOCs) and of suppression of Pythium impacts on Hyacinth root development. One year later, the composition of the bacterial community in the AD soils was reflecting that of the untreated soils. In addition, both production of Pythium-suppressing VOCs and suppression of Pythium in Hyacinth bioassays had returned to the levels of the untreated soil. GC/MS analysis identified several VOCs, among which compounds known to be antifungal, that were produced in the untreated soils but not in the AD soils. These compounds were again produced 15 months after the AD treatment. Our data indicate that soils exposed to a drastic stress can temporarily lose pathogen suppressive characteristics and that both loss and return of these suppressive characteristics coincides with shifts in the soil bacterial community composition. Our data are supporting the suggested importance of microbial VOCs in the natural buffer of soils against diseases caused by soil-borne pathogens.

Airborne medicine: bacterial volatiles and their influence on plant health

“…This suggests that these compounds might contribute to the ‘disease suppressiveness’ of soils (low disease incidence occurring despite the presence of a virulent pathogen), although this property has been traditionally linked to nonvolatile bacterial metabolites such as 2,4‐diacetylphloroglucinol (Weller et al , ). Indeed, a recent study revealed that changes in soil bacterial community composition caused by anaerobic disinfestation coincided with a loss of emission of Pythium suppressing volatiles and with an increase of hyacinth root infection by the same pathogen (van Agtmaal et al , ).…”

The ecological role of volatile mediated interactions belowground

“…The relationship between community composition and VOCs production is in accordance with previous studies (Garbeva et al 2014a;Hol et al 2015;Tyc et al 2015;Van Agtmaal et al 2015;El Ariebi et al 2016). In this regard, the presence of low-abundant species in the microbial community, such as observed for the Paenibacillus strain in Chapter 3, can significantly contribute to the emission of certain VOCs such as pyrazines with antifungal activity .…”

Mining into interspecific bacterial interactions

“…Many studies have shown that bacterial volatiles play a major role in the suppression of soil-borne fungi (Zou et al, 2007;Garbeva et al, 2011a;van Agtmaal et al, 2015). In chapter four I also detected strong anti-fungal and anti-oomycetal activity caused by the volatile blends produced by the four tested bacteria cultivated in monocultures or mixed cultures.…”

“…The high amount of dimethyl di-and trisulfide detected in both monocultures and interactions indicate that these compounds are commonly produced. Many studies have shown that bacterial volatiles play a major role in soil fungistasis (Zou et al, 2007;Garbeva et al, 2011a;Garbeva et al, 2014b;van Agtmaal et al, 2015).…”