The antifungal and other bioactive properties of the volatilome of Streptomyces scabiei
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Abstract
Volatile compounds (VCs) produced by most host-associated bacteria remain largely unexplored despite their potential roles in suppressing microbial competitors and facilitating host colonization. This study investigated the volatilome of Streptomyces scabiei 87-22, the model species for causative agents of common scab in root and tuber crops, under culture conditions that completely inhibited fungal growth, including the phytopathogens Alternaria solani and Gibberella zeae . Bicameral assays confirmed that these inhibitory effects were at least partially mediated by VCs. Using GC × GC TOFMS, 36 VCs were unambiguously identified as products of S . scabiei 87-22 metabolic activity. These included mainly ketones and aromatic compounds (both benzene derivatives and heterocycles), along with smaller contributions from other chemical families including sulfur-containing compounds, nitriles, esters, terpenoids, an amide, and an aldehyde. A literature survey suggests that many of these VCs possess antibacterial, antifungal, anti-oomycete, nematocidal, and insecticidal effects, while the bioactivity of others remains speculative, having been identified only within complex volatile mixtures. Among those with known antifungal properties, dimethyl trisulfide, 2-heptanone, and creosol inhibited the growth of the fungal pathogens tested in this study. In addition, we reveal here that 3-penten-2-one is also a strong inhibitor of fungal growth. Remarkably, despite S . scabiei 87-22 being defined as a pathogen, some of its VCs were associated with plant growth promotion and defense stimulation. Overall, our work highlights the remarkable potential of S . scabiei 87-22 to produce VCs with diverse bioactivities including fungal pathogen inhibition and priming plant resistance.
Importance
This study reveals that Streptomyces scabiei , the bacterium causing common scab in root and tuber crops, produces a wide variety of volatile chemicals with surprising benefits. These natural compounds can inhibit growth of other harmful microbes, including fungal plant pathogens. Some of these chemicals are already known to fight pests and diseases, while others, like 3-penten-2-one, are newly discovered as potential antifungals. Even more unexpectedly, some of the identified compounds may help plants grow or boost their defenses. Combined with previous work, our findings challenge the idea that S . scabiei is purely harmful and suggests it might, under certain conditions, play a protective role in its environment. This work deepens our understanding of how microbes interact with each other and with plants, and could help shape more sustainable approaches to agriculture.
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n addition, S. scabiei 87-22 produces numerous other compounds known for their antimicrobial activity against a broader range of fungi and bacteria.
It would be great to add either here or in the introduction more context around S. scabiei. What do we know about its metabolic potential? If it is a model, is its genome sequenced, and if so, are there other things you could do to support your hypotheses around the VCs having antifungal impacts? Do you know the genes responsible for production of any of these compounds and are these genes present? Could you compare the expression of these genes in isolation/coculture ?
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previously reported for their antimicrobial properties
If you have a couple candidate VCs that you think are driving what you observe in your growth assays, it would be great to measure the production of these in isolates vs. fungal coculture
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he 12 VCs that have previously been reported for their antimicrobial properties (Table 1).
Based on your lit review, are any of these VCs associated with Strep species? It would be nice to put into your table the biological system that this was observed in . Are they all examples where the VC is produced by bacteria?
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MHB
Should this be MHA? Same for TSB/TSA? If this is a broth vs agar thing, it seems like these should be agar?
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volatilome of S. scabiei 87-22 across the five culture conditions tested (MHB, LB, ISP6, TSB, and ISP1)
Have you done any work looking at the volatiles produced during coculture? If this is an antifungal , it seems like production may be tied to the presence of fungi. I understand this may be challenging to do in liquid with molds, but I suspect there are creative ways to solve this that you could find in the literature around VOCs in microbial interactions
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A), and MHB (liquid MHA) (not shown)
It would be good to include the data here if you think this was a crucial step, as you mention in the next sentence. At the very least, it would be nice to state how you confirmed it.
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The VCs produced in ISP1, ISP6, LB, TSA, and MHA media resulted in complete inhibition of
How long after inoculation were these images taken? Can you comment on how this relates to the growth rates of these different organisms? Are the control plates imaged at the same timepoint>?
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Pe. restrictum NS1.
Why did you choose to do a dilution series with Pe. restricum? It may have been nice to capture the interaction earlier on, as right now the outcome seems binary (growth/ no growth)
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score of 100 means full growth inhibition of the tested microorganism
I assume this is in the methods, but it would be nice to add here how these scores are determined (I assume you measured something?). The pictures are helpful but It is hard to interpret the scores in the figure without understanding what they are coming from
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ISP1, ISP6, LB, TSA, and MHA
It would also be nice to comment on why you chose these media. For example, if they are Strep specific media that you expect may increase antibiotic production, etc.
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Figure 1.
small note that this figure is very blurry, even when downloaded
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growth of various fungal and oomycete microorganisms,
Could you comment briefly on why you chose this panel of fungal strains? It seems from your methods that they come from various culture collections, but it would be nice to have a little information here on where they were originally isolated from and whether you expect to find Streptomyces scabiei in those same environments. Are these fungi particularly agriculturally relevant as candidates for a VOC pesticide (in terms of total crop losses, or for a specific crop, or because they lack other effective control measures?)
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