Abstract
To develop more ecologically sustainable agricultural practices requires that we reduce our reliance on synthetic chemical pesticides for crop protection. This will likely involve optimized biocontrol approaches – the use of beneficial soil microbes to attack potential plant pathogens to protect plants from diseases. Many bacterial species, including strains of Bacillus subtilis, have been explored for their biocontrol properties, as they can control the growth of harmful fungi, often by disrupting the fungal cell wall. A strain that is not often considered for this particular application is Bacillus subtilis natto, primarily known for fermenting soybeans via cell wall degradation in the Japanese probiotic dish “natto.” Because deconstruction of the fungal cell wall is considered an important biocontrol trait, we were motivated to explore the possible anti-fungal properties of the B. subtilis natto strain. We show that B. subtilis natto can use complex fungal material as a carbon source for growth, and can effectively deconstruct fungal cell walls. We found degradation of fungal cell wall proteins, and showed that growth on a mix of peptides was very strong. We also found that intact fungal cell walls can induce the secretion of chitinases and proteases. Surprisingly, we could show that chitin, the bulk component of the fungal cell wall, does not permit successful growth of the natto strain or induce the secretion of chitinolytic enzymes, although these were produced during exposure to proteins or to complex fungal material. We have further shown that protease secretion is likely a constitutively enabled mechanism for nutrient scavenging by B. subtilis natto, as well as a potent tool for the degradation of fungal cell walls. Overall, our data highlight B. subtilis natto as a promising candidate for biocontrol products, with relevant behaviors that can be optimized by altering growth conditions. Whereas it is common for bacterial biocontrol products to be supplied with chitin or chitosan as a priming polysaccharide, our data indicate that this is not a useful approach with this particular bacterium, which should instead be supplied with either glucose or attenuated fungal material.
Highlights
One of the greatest threats to global food security is the massive loss of staple crops to fungal disease (Dean et al, 2012; Fisher et al, 2012)
We first investigated the ability of B. subtilis natto to grow on fungal fruiting body (FB), extracted fungal cell wall (FCW), and the two major Fungal cell wall (FCW) carbohydrates – chitin and β-glucan – as sole carbon source
Cultures were sampled regularly for up to 26 h, and optical density (OD) was measured as an indicator of culture turbidity. All of these conditions were studied both with and without the additional presence of 5 g L−1 glucose. This experimental set-up allowed us to investigate the potential for degradation of FCW and its components even when not being used as the primary carbon source supporting growth
Summary
One of the greatest threats to global food security is the massive loss of staple crops to fungal disease (Dean et al, 2012; Fisher et al, 2012). Synthetic pesticides are often found at high levels in soil and water, and accumulate in food webs with increasing toxicity (Damalas and Eleftherohorinos, 2011; Jorgensen et al, 2012; Silva et al, 2019). This poses risks to environmental and human health, and contributes to the increasing incidence of fungal resistance to chemical pesticides (Deising et al, 2008; Price et al, 2015; Hawkins et al, 2018). One popular suggestion is to increase the efficacy of biocontrol, which is the use of living organisms to control plant disease vectors This includes certain bacteria that are naturally able to limit the growth of phytopathogenic fungi. Biocontrol bacteria are often packaged together with chitin, which has long been thought to prime their anti-fungal behaviors (Sid Ahmed et al, 2003; Kokalis-Burelle et al, 2006; Yandigeri et al, 2015)
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