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Biocontrol agents promote growth of potato pathogens, depending on environmental conditions.

Cray JA, Connor MC, Stevenson A, Houghton JD, Rangel DE, Cooke LR, Hallsworth JE - Microb Biotechnol (2016)

Bottom Line: Whilst unprecedented, this finding is consistent with earlier reports that fungi can utilize metabolites derived from bacterial cells.Unless the antimicrobial activities of candidate biocontrol strains are assayed over a full range of field-relevant parameters, biocontrol agents may promote plant pathogen infections and thereby reduce crop yields.These findings indicate that biocontrol activity, therefore, ought to be regarded as a mode-of-behaviour (dependent on prevailing conditions) rather than an inherent property of a bacterial strain.

View Article: PubMed Central - PubMed

Affiliation: Institute for Global Food Security, School of Biological Sciences, MBC, Queen's University Belfast, Belfast, BT9 7BL, Northern Ireland.

No MeSH data available.


Related in: MedlinePlus

Radial extension of Fusarium coeruleum colonies when cultured alone (●) and during inhibition assays with Bacillus sp. JC12GB43, (●): on (A) PDA with no added solute; (B and C) PDA supplemented with urea; and (D–F) PDA supplemented with glycerol, at 20°C. Urea was incorporated into media at concentrations of 68.4 mM (b) and 132 mM (C); glycerol was incorporated at concentrations of 1.84 M (D), 2.17 M (E) and 2.53 (F). Fusarium coeruleum and Bacillus sp. JC12GB43 were inoculated 15‐mm apart, and error bars indicate ± standard error.
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mbt212349-fig-0007: Radial extension of Fusarium coeruleum colonies when cultured alone (●) and during inhibition assays with Bacillus sp. JC12GB43, (●): on (A) PDA with no added solute; (B and C) PDA supplemented with urea; and (D–F) PDA supplemented with glycerol, at 20°C. Urea was incorporated into media at concentrations of 68.4 mM (b) and 132 mM (C); glycerol was incorporated at concentrations of 1.84 M (D), 2.17 M (E) and 2.53 (F). Fusarium coeruleum and Bacillus sp. JC12GB43 were inoculated 15‐mm apart, and error bars indicate ± standard error.

Mentions: Interaction assays were carried out on media supplemented with solutes known to be permissive for growth of the biocontrol agents (Table 1); i.e. glycerol or NaCl. The media used for this purpose were NA+1.583 M glycerol (0.958 water activity) and NA+1.104 M NaCl (0.961 water activity); each of the biocontrol agents assayed (JC12GB6, JC12GB7, JC12GB12, JC12GB13, JC12GB14, JC12GB189 JC12GB190, JC12GB191, JC12GB196 and JC12GB197) had been isolated using one of these media (Fig. 5; Fig. S5). On these reduced water‐activity media, both the colony expansion of biocontrol agent strains, and radial growth rates of potato pathogens were decreased (Fig. 5) relative to those on high water‐activity media (Fig. 1). Importantly, despite the low water activity, the colonies of biocontrol agent strains JC12GB7, JC12GB12, JC12GB13 and JC12GB14 expanded rapidly (Fig. 5B), indicating potential for effective biocontrol at reduced water availability. Furthermore, these four isolates achieved medium coverage by forming a bacterial lawn (Fig. 5B). However, the biocontrol strains JC12GB12 and JC12GB7 (Fig. 5A) exhibited poor inhibition coefficients under these conditions; in the range 10–16 (Fig. 2B; Table S1). Interestingly, strains assayed on glycerol‐supplemented media were generally inhibitory to F. coeruleum, whereas those assayed on NaCl‐supplemented media induced a slight promotion of fungal growth (Fig. 5A and D). Bacillus sp. JC12GB43:F. coeruleum interaction assays using Bacillus inocula that had been cultured at 2 M glycerol (the chaotropic activity and water activity of the Bacillus pre‐culture medium = 3.28 kJ kg−1 and 0.955 respectively), i.e. Treatment 3 was carried out to determine the inhibitory potency of this biocontrol agent during the infection process on the potato tuber. Surprisingly, however, there was a promotion of the tuber F. coeruleum infection of tubers for treatments inoculated with the Bacillus sp. JC12GB43, 2‐M glycerol inoculum (Fig. 6). This promotion of the pathogen colony ranged from 65% to 570% relative to the level of infection observed in the control (control tubers were wounded and inoculated with F. coeruleum; no biocontrol agent) (Fig. 6). Although NB+glycerol inoculations were also of benefit to the pathogen (Fig. 6), this NB+2 M glycerol treatment (Treatment 2) had not been used as a culture medium and so did not have depleted levels of glycerol (some of which can be lost through evaporation during the incubation period, thereby increasing the water activity). The low water activity of Treatment 2, therefore, may have stressed and weakened the potato cells, slowed wound‐healing and thereby enhanced pathogen infection (wounded potato cells are highly metabolically active and susceptible to abiotic stresses; Morelli et al., 1998). Furthermore, the outcome for Treatment 2 in the in‐vivo assay was the converse of the outcome observed for the in‐vitro assay (Fig. 7D–F; Table S5). The in‐vivo Bacillus sp. JC12GB43:F. coeruleum interaction assay does, nevertheless, raise the possibility that formulation of biocontrol agents in either glycerol or other low molecular‐mass solutes (Torres et al., 2003; Bora et al., 2004; Patiño‐Vera et al., 2005) may potentially reduce or even reverse the biocontrol potential of microbial agents used in the field; more work is needed to confirm this.


Biocontrol agents promote growth of potato pathogens, depending on environmental conditions.

Cray JA, Connor MC, Stevenson A, Houghton JD, Rangel DE, Cooke LR, Hallsworth JE - Microb Biotechnol (2016)

Radial extension of Fusarium coeruleum colonies when cultured alone (●) and during inhibition assays with Bacillus sp. JC12GB43, (●): on (A) PDA with no added solute; (B and C) PDA supplemented with urea; and (D–F) PDA supplemented with glycerol, at 20°C. Urea was incorporated into media at concentrations of 68.4 mM (b) and 132 mM (C); glycerol was incorporated at concentrations of 1.84 M (D), 2.17 M (E) and 2.53 (F). Fusarium coeruleum and Bacillus sp. JC12GB43 were inoculated 15‐mm apart, and error bars indicate ± standard error.
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mbt212349-fig-0007: Radial extension of Fusarium coeruleum colonies when cultured alone (●) and during inhibition assays with Bacillus sp. JC12GB43, (●): on (A) PDA with no added solute; (B and C) PDA supplemented with urea; and (D–F) PDA supplemented with glycerol, at 20°C. Urea was incorporated into media at concentrations of 68.4 mM (b) and 132 mM (C); glycerol was incorporated at concentrations of 1.84 M (D), 2.17 M (E) and 2.53 (F). Fusarium coeruleum and Bacillus sp. JC12GB43 were inoculated 15‐mm apart, and error bars indicate ± standard error.
Mentions: Interaction assays were carried out on media supplemented with solutes known to be permissive for growth of the biocontrol agents (Table 1); i.e. glycerol or NaCl. The media used for this purpose were NA+1.583 M glycerol (0.958 water activity) and NA+1.104 M NaCl (0.961 water activity); each of the biocontrol agents assayed (JC12GB6, JC12GB7, JC12GB12, JC12GB13, JC12GB14, JC12GB189 JC12GB190, JC12GB191, JC12GB196 and JC12GB197) had been isolated using one of these media (Fig. 5; Fig. S5). On these reduced water‐activity media, both the colony expansion of biocontrol agent strains, and radial growth rates of potato pathogens were decreased (Fig. 5) relative to those on high water‐activity media (Fig. 1). Importantly, despite the low water activity, the colonies of biocontrol agent strains JC12GB7, JC12GB12, JC12GB13 and JC12GB14 expanded rapidly (Fig. 5B), indicating potential for effective biocontrol at reduced water availability. Furthermore, these four isolates achieved medium coverage by forming a bacterial lawn (Fig. 5B). However, the biocontrol strains JC12GB12 and JC12GB7 (Fig. 5A) exhibited poor inhibition coefficients under these conditions; in the range 10–16 (Fig. 2B; Table S1). Interestingly, strains assayed on glycerol‐supplemented media were generally inhibitory to F. coeruleum, whereas those assayed on NaCl‐supplemented media induced a slight promotion of fungal growth (Fig. 5A and D). Bacillus sp. JC12GB43:F. coeruleum interaction assays using Bacillus inocula that had been cultured at 2 M glycerol (the chaotropic activity and water activity of the Bacillus pre‐culture medium = 3.28 kJ kg−1 and 0.955 respectively), i.e. Treatment 3 was carried out to determine the inhibitory potency of this biocontrol agent during the infection process on the potato tuber. Surprisingly, however, there was a promotion of the tuber F. coeruleum infection of tubers for treatments inoculated with the Bacillus sp. JC12GB43, 2‐M glycerol inoculum (Fig. 6). This promotion of the pathogen colony ranged from 65% to 570% relative to the level of infection observed in the control (control tubers were wounded and inoculated with F. coeruleum; no biocontrol agent) (Fig. 6). Although NB+glycerol inoculations were also of benefit to the pathogen (Fig. 6), this NB+2 M glycerol treatment (Treatment 2) had not been used as a culture medium and so did not have depleted levels of glycerol (some of which can be lost through evaporation during the incubation period, thereby increasing the water activity). The low water activity of Treatment 2, therefore, may have stressed and weakened the potato cells, slowed wound‐healing and thereby enhanced pathogen infection (wounded potato cells are highly metabolically active and susceptible to abiotic stresses; Morelli et al., 1998). Furthermore, the outcome for Treatment 2 in the in‐vivo assay was the converse of the outcome observed for the in‐vitro assay (Fig. 7D–F; Table S5). The in‐vivo Bacillus sp. JC12GB43:F. coeruleum interaction assay does, nevertheless, raise the possibility that formulation of biocontrol agents in either glycerol or other low molecular‐mass solutes (Torres et al., 2003; Bora et al., 2004; Patiño‐Vera et al., 2005) may potentially reduce or even reverse the biocontrol potential of microbial agents used in the field; more work is needed to confirm this.

Bottom Line: Whilst unprecedented, this finding is consistent with earlier reports that fungi can utilize metabolites derived from bacterial cells.Unless the antimicrobial activities of candidate biocontrol strains are assayed over a full range of field-relevant parameters, biocontrol agents may promote plant pathogen infections and thereby reduce crop yields.These findings indicate that biocontrol activity, therefore, ought to be regarded as a mode-of-behaviour (dependent on prevailing conditions) rather than an inherent property of a bacterial strain.

View Article: PubMed Central - PubMed

Affiliation: Institute for Global Food Security, School of Biological Sciences, MBC, Queen's University Belfast, Belfast, BT9 7BL, Northern Ireland.

No MeSH data available.


Related in: MedlinePlus