TY - JOUR
T1 - Competition sensing changes antibiotic production in streptomyces
AU - Westhoff, Sanne
AU - Kloosterman, Alexander M.
AU - van Hoesel, Stephan F.A.
AU - van Wezel, Gilles P.
AU - Rozen, Daniel E.
N1 - Funding Information:
This work was financially supported by grants 824.02.003 and 731.014.206 from the Dutch National Science Foundation (NWO) to D.E.R. and to G.P.v.W., respectively. The authors contributed in the following ways. S.W. and D.E.R. designed the experiments. S.W. performed the experiments and analyzed the data. A.K. and S.F.A.v.H. assisted with the (bio)informatics. S.W., D.E.R., and G.P.v.W. wrote the manuscript. We declare there is no conflict of interest.
Publisher Copyright:
© 2021 Westhoff et al.
PY - 2021
Y1 - 2021
N2 - One of the most important ways that bacteria compete for resources and space is by producing antibiotics that inhibit competitors. Because antibiotic production is costly, the biosynthetic gene clusters coordinating their synthesis are under strict regulatory control and often require “elicitors” to induce expression, including cues from competing strains. Although these cues are common, they are not produced by all competitors, and so the phenotypes causing induction remain unknown. By studying interactions between 24 antibiotic-producing strains of strep-tomycetes, we show that strains commonly inhibit each other’s growth and that this occurs more frequently if strains are closely related. Next, we show that antibiotic production is more likely to be induced by cues from strains that are closely related or that share secondary metabolite biosynthetic gene clusters (BGCs). Unexpectedly, antibiotic production is less likely to be induced by competitors that inhibit the growth of a focal strain, indicating that cell damage is not a general cue for induction. In addition to induction, antibiotic production often decreases in the presence of a competitor, although this response was not associated with genetic relatedness or overlap in BGCs. Finally, we show that resource limitation increases the chance that antibiotic production declines during competition. Our results reveal the importance of social cues and resource availability in the dynamics of interference competition in streptomycetes. IMPORTANCE Bacteria secrete antibiotics to inhibit their competitors, but the presence of competitors can determine whether these toxins are produced. Here, we study the role of the competitive and resource environment on antibiotic production in Streptomyces, bacteria renowned for their production of antibiotics. We show that Streptomyces cells are more likely to produce antibiotics when grown with competitors that are closely related or that share biosynthetic pathways for secondary metabo-lites, but not when they are threatened by competitor’s toxins, in contrast to predictions of the competition sensing hypothesis. Streptomyces cells also often reduce their output of antibiotics when grown with competitors, especially under nutrient limita-tion. Our findings highlight that interactions between the social and resource environ-ments strongly regulate antibiotic production in these medicinally important bacteria.
AB - One of the most important ways that bacteria compete for resources and space is by producing antibiotics that inhibit competitors. Because antibiotic production is costly, the biosynthetic gene clusters coordinating their synthesis are under strict regulatory control and often require “elicitors” to induce expression, including cues from competing strains. Although these cues are common, they are not produced by all competitors, and so the phenotypes causing induction remain unknown. By studying interactions between 24 antibiotic-producing strains of strep-tomycetes, we show that strains commonly inhibit each other’s growth and that this occurs more frequently if strains are closely related. Next, we show that antibiotic production is more likely to be induced by cues from strains that are closely related or that share secondary metabolite biosynthetic gene clusters (BGCs). Unexpectedly, antibiotic production is less likely to be induced by competitors that inhibit the growth of a focal strain, indicating that cell damage is not a general cue for induction. In addition to induction, antibiotic production often decreases in the presence of a competitor, although this response was not associated with genetic relatedness or overlap in BGCs. Finally, we show that resource limitation increases the chance that antibiotic production declines during competition. Our results reveal the importance of social cues and resource availability in the dynamics of interference competition in streptomycetes. IMPORTANCE Bacteria secrete antibiotics to inhibit their competitors, but the presence of competitors can determine whether these toxins are produced. Here, we study the role of the competitive and resource environment on antibiotic production in Streptomyces, bacteria renowned for their production of antibiotics. We show that Streptomyces cells are more likely to produce antibiotics when grown with competitors that are closely related or that share biosynthetic pathways for secondary metabo-lites, but not when they are threatened by competitor’s toxins, in contrast to predictions of the competition sensing hypothesis. Streptomyces cells also often reduce their output of antibiotics when grown with competitors, especially under nutrient limita-tion. Our findings highlight that interactions between the social and resource environ-ments strongly regulate antibiotic production in these medicinally important bacteria.
KW - Antibiotic production
KW - Interference competition
KW - Microbial ecology
KW - Social microbiology
KW - Streptomyces
U2 - 10.1128/mBio.02729-20
DO - 10.1128/mBio.02729-20
M3 - Article
C2 - 33563841
AN - SCOPUS:85100555541
SN - 2161-2129
VL - 12
SP - 1
EP - 13
JO - mBio
JF - mBio
IS - 1
M1 - e02729-20
ER -