Biosynthetic gene cluster profiling predicts the positive association between antagonism and phylogeny in Bacillus

Understanding the driving forces and intrinsic mechanisms of microbial competition is a fundamental question in microbial ecology. Despite the well-established negative correlation between exploitation competition and phylogenetic distance, the process of interference competition that is exemplified by antagonism remains controversial. Here, we studied the genus Bacillus, a commonly recognized producer of multifarious antibiotics, to explore the role of phylogenetic patterns of biosynthetic gene clusters (BGCs) in mediating the relationship between antagonism and phylogeny. Comparative genomic analysis revealed a positive association between BGC distance and phylogenetic distance. Antagonistic tests demonstrated that the inhibition phenotype positively correlated with both phylogenetic and predicted BGC distance, especially for antagonistic strains possessing abundant BGCs. Mutant-based verification showed that the antagonism was dependent on the BGCs that specifically harbored by the antagonistic strain. These findings highlight that BGC-phylogeny coherence regulates the positive correlation between congeneric antagonism and phylogenetic distance, which deepens our understanding of the driving force and intrinsic mechanism of microbial interactions.

Mechanisms Involved in Interspecific Communication between Wine Yeasts

In parallel with the development of non-Saccharomyces starter cultures in oenology, a growing interest has developed around the interactions between the microorganisms involved in the transformation of grape must into wine. Nowadays, it is widely accepted that the outcome of a fermentation process involving two or more inoculated yeast species will be different from the weighted average of the corresponding individual cultures. Interspecific interactions between wine yeasts take place on several levels, including interference competition, exploitation competition, exchange of metabolic intermediates, and others. Some interactions could be a simple consequence of each yeast running its own metabolic programme in a context where metabolic intermediates and end products from other yeasts are present. However, there are clear indications, in some cases, of specific recognition between interacting yeasts. In this article we discuss the mechanisms that may be involved in the communication between wine yeasts during alcoholic fermentation.

Is Exploitation Competition Involved in a Multitrophic Strategy for the Biocontrol of Fusarium Head Blight?

Trichoderma gamsii T6085 was used in combination with a Fusarium oxysporum isolate (7121) in order to evaluate, in a multitrophic approach, their competitive ability against F. graminearum, one of the main causal agents of Fusarium head blight (FHB) on wheat. The two antagonists and the pathogen were coinoculated on two different natural substrates, wheat and rice kernels. Both T6085 and 7121, alone and coinoculated, significantly reduced the substrate colonization and mycotoxin production by the pathogen. The two antagonists did not affect each other. Using a metabolic approach (Biolog), we investigated whether exploitation competition could explain this antagonistic activity. The aim was to define whether the three fungi coexist or if one isolate nutritionally dominates another. Results obtained from Biolog suggest that no exploitative competition occurs between the antagonists and the pathogen during the colonization of the natural substrates. Interference competition was then preliminarily evaluated to justify the reduction in the pathogen’s growth and to better explain mechanisms. A significant reduction of F. graminearum growth was observed when the pathogen grew in the cultural filtrates of T. gamsii T6085, both alone and cocultured with F. oxysporum 7121, thus suggesting the involvement of secondary metabolites. As far as we know, this is the first time that an ecological study has been performed to explain how and which kind of competition could be involved in a multitrophic biocontrol of FHB.

Competition among Nasal Bacteria Suggests a Role for Siderophore-Mediated Interactions in Shaping the Human Nasal Microbiota

ABSTRACTResources available in the human nasal cavity are limited. Therefore, to successfully colonize the nasal cavity, bacteria must compete for scarce nutrients. Competition may occur directly through interference (e.g., antibiotics) or indirectly by nutrient sequestration. To investigate the nature of nasal bacterial competition, we performed coculture inhibition assays between nasalActinobacteriaandStaphylococcusspp. We found that isolates of coagulase-negative staphylococci (CoNS) were sensitive to growth inhibition byActinobacteriabut thatStaphylococcus aureusisolates were resistant to inhibition. AmongActinobacteria, we observed thatCorynebacteriumspp. were variable in their ability to inhibit CoNS. We sequenced the genomes of 10Corynebacteriumspecies isolates, including 3Corynebacterium propinquumisolates that strongly inhibited CoNS and 7 otherCorynebacteriumspecies isolates that only weakly inhibited CoNS. Using a comparative genomics approach, we found that theC. propinquumgenomes were enriched in genes for iron acquisition and harbored a biosynthetic gene cluster (BGC) for siderophore production, absent in the noninhibitoryCorynebacteriumspecies genomes. Using a chrome azurol S assay, we confirmed thatC. propinquumproduced siderophores. We demonstrated that iron supplementation rescued CoNS from inhibition byC. propinquum, suggesting that inhibition was due to iron restriction through siderophore production. Through comparative metabolomics and molecular networking, we identified the siderophore produced byC. propinquumas dehydroxynocardamine. Finally, we confirmed that the dehydroxynocardamine BGC is expressedin vivoby analyzing human nasal metatranscriptomes from the NIH Human Microbiome Project. Together, our results suggest that bacteria produce siderophores to compete for limited available iron in the nasal cavity and improve their fitness.IMPORTANCEWithin the nasal cavity, interference competition through antimicrobial production is prevalent. For instance, nasalStaphylococcusspecies strains can inhibit the growth of other bacteria through the production of nonribosomal peptides and ribosomally synthesized and posttranslationally modified peptides. In contrast, bacteria engaging in exploitation competition modify the external environment to prevent competitors from growing, usually by hindering access to or depleting essential nutrients. As the nasal cavity is a nutrient-limited environment, we hypothesized that exploitation competition occurs in this system. We determined thatCorynebacterium propinquumproduces an iron-chelating siderophore, and this iron-sequestering molecule correlates with the ability to inhibit the growth of coagulase-negative staphylococci. Furthermore, we found that the genes required for siderophore production are expressedin vivo. Thus, although siderophore production by bacteria is often considered a virulence trait, our work indicates that bacteria may produce siderophores to compete for limited iron in the human nasal cavity.

Bacterial competition mediated by siderophore production among the human nasal microbiota

ABSTRACTResources available in the human nasal cavity are limited. Therefore, to successfully colonize the nasal cavity, bacteria must compete for scarce nutrients. Competition may occur directly through interference (e.g., antibiotics) or indirectly by nutrient sequestration. To investigate the nature of nasal bacterial competition, we performed co-culture inhibition assays between nasal Actinobacteria andStaphylococcusspp. We found thatStaphylococcus epidermidisisolates were sensitive to growth inhibition by Actinobacteria butStaphylococcus aureusisolates were resistant to inhibition. Among Actinobacteria, we observed thatCorynebacteriumspp. were variable in their ability to inhibitS. epidermidis.We sequenced the genomes of tenCorynebacteriumspp. isolates, including threeCorynebacterium propinquumthat strongly inhibitedS. epidermidisand seven otherCorynebacteriumspp. isolates that only weakly inhibitedS. epidermidis.Using a comparative genomics approach, we found that theC. propinquumgenomes were enriched in genes for iron acquisition and encoded a biosynthetic gene cluster (BGC) for siderophore production, absent in the non-inhibitoryCorynebacteriumspp. genomes. Using a chromeazurol S assay, we confirmed thatC. propinquumproduced siderophores. We demonstrated that iron supplementation rescuedS. epidermidisfrom inhibition byC. propinquum, suggesting that inhibition was due to iron restriction through siderophore production. Using comparative metabolomics, we identified the siderophore produced byC. propinquumas dehydroxynocardamine. Finally, we confirmed that the dehydroxynocardamine BGC is expressedin vivoby analyzing human nasal metatranscriptomes from the NIH Human Microbiome Project.Together, our results suggest that bacteria produce siderophores to compete for limited available iron in the nasal cavity and improve their fitness.IMPORTANCEWithin the nasal cavity, interference competition through antimicrobial production is prevalent. For instance, nasalStaphylococcusspp. strains can inhibit the growth of other bacteria through the production of nonribosomal peptides and ribosomally synthesized and post-translationally modified peptides. In contrast, bacteria engaging in exploitation competition modify the external environment to prevent competitors from growing, usually by depleting access to essential nutrients. As the nasal cavity is a nutrient limited environment, we hypothesized that exploitation competition occurs in this system. We determined thatCorynebacterium propinquumproduces an iron-chelating siderophore and is able to use this molecule to sequester iron and inhibit the growth ofStaphylococcus epidermidis.Further, we found that the genes required for siderophore production are expressedin vivo.Thus, though siderophore production by bacteria is often considered a virulence trait, our work indicates that bacteria may produce siderophores to compete for limited iron in the human nasal cavity.

Interference competition pressure predicts the number of avian predators that shifted their timing of activity

Being active at different times facilitates the coexistence of functionally similar species. Hence, time partitioning might be induced by competition. However, the relative importance of direct interference and indirect exploitation competition on time partitioning remains unclear. The aim of this study was to investigate the relative importance of these two forms of competition on the occurrence of time-shifting among avian predator species. As a measure of interference competition pressure, we used the species richness of day-active avian predator species or of night-active avian predator species (i.e. species of Accipitriformes, Falconiformes and Strigiformes) in a particular geographical area (assemblage). As an estimate of exploitation competition pressure, we used the total species richness of avian predators in each assemblage. Estimates of the intensity of interference competition robustly predicted the number of Accipitriformes species that became crepuscular and the number of Strigiformes species that became day-active or strictly crepuscular. Interference competition pressure may depend on body size and on the total duration of the typical active period (day or night length). Our results support—to some extent—that smaller species are more likely to become time-shifters. Day length did not have an effect on the number of time-shifter species in the Accipitriformes. Among the large Strigiformes, more time-shifter species occur in areas where nights are shorter (i.e. where less of the typical time resource is available). However, in the small Strigiformes, we found the opposite, counterintuitive effect: more time-shifters where nights are longer. Exploitation competition may have had an additional positive effect on the number of time-shifters, but only in Accipitriformes, and the effect was not as robust. Our results thus support the interference competition hypothesis, suggesting that animals may have shifted their time of activity, despite phylogenetic constraints on the ability to do so, to reduce the costs of direct interactions. Our findings also highlight the influence of body size as a surrogate of competitive ability during encounters on time partitioning, at least among avian predators.