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Kummerli, R.

Publications and source records attributed to Kummerli, R..

6 recordsLinked to original sources

Utilization of cyanobacterial siderophore cyanochelin B by phylogenetically distant heterotrophs suggest its role in mediating microbial interactions

Cyanobacteria are key prokaryotic primary producers in diverse ecosystems, yet the role of cyanobacterial siderophores in shaping their associated microbiomes remains unexplored. Our study demonstrates the benefits provided to the heterotrophic co-habitants of filamentous cyanobacteria in terrestrial microbial biofilms, focusing on the recently discovered widespread siderophores cyanochelins. To address the acceptance of cyanochelin B (CychB) across multiple bacterial classes, we first investigated its role in providing iron to a model siderophore producer P. aeruginosa PAO1 and selected Pseudomonas natural isolates, which were found to utilize CychB under iron limiting conditions while downregulating endogenous siderophore production. In response to CychB, PAO1 expresses a siderophore internalization cluster, which is localized in multiple Pseudomonas natural isolates. Using metagenome analysis, we characterized the bacterial community recruited along with CychB producing Phormidesmis cyanobacteria under long-term iron starvation. Potential CychB acceptor bacteria associated with the CychB producer were predominantly lacking endogenous siderophore machineries. Using siderophore selective pressure, we isolated a genuine CychB acceptor, gram-negative bacterium Methyloversatilis sp. S146 and demonstrated that its genome hosts an iron processing cluster overexpressed after CychB feeding, recognizing Methyloversatilis as a candidate for further mechanistic investigation of iron acquisition-driven microbial interactions. Our results indicate that CychB supports a specific subset of co-habiting heterotrophic bacteria during iron starvation, further emphasizing the role of cyanobacteria as key drivers of nutrient flows within globally important microbial soil crust ecosystems, supporting microbial life in nutrient-limited environments. These findings provide a mechanistic foundation to elucidate the role of cyanochelins as a public good in these communities.

microbiology↗

From sequence to molecules: Feature sequence-based genome mining uncovers the hidden diversity of bacterial siderophore pathways

Microbial secondary metabolites are a rich source for pharmaceutical discoveries and play crucial ecological functions. While tools exist to identify secondary metabolite clusters in genomes, precise sequence-to-function mapping remains challenging because neither function nor substrate specificity of biosynthesis enzymes can accurately be predicted. Here we developed a knowledge-guided bioinformatic pipeline to solve these issues. We analyzed 1928 genomes of Pseudomonas bacteria and focused on iron-scavenging pyoverdines as model metabolites. Our pipeline predicted 188 chemically different pyoverdines with nearly 100% structural accuracy and the presence of 94 distinct receptor groups required for the uptake of iron-loaded pyoverdines. Our pipeline unveils an enormous yet overlooked diversity of siderophores (151 new structures) and receptors (91 new groups). Our approach, combining feature sequence with phylogenetic approaches, is extendable to other metabolites and microbial genera, and thus emerges as powerful tool to reconstruct bacterial secondary metabolism pathways based on sequence data. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=118 SRC="FIGDIR/small/564663v5_ufig1.gif" ALT="Figure 1"> View larger version (20K): org.highwire.dtl.DTLVardef@1dedad4org.highwire.dtl.DTLVardef@1f0a39eorg.highwire.dtl.DTLVardef@185e345org.highwire.dtl.DTLVardef@10beec6_HPS_FORMAT_FIGEXP M_FIG C_FIG

genomics↗

Transposable temperate phages promote the evolution of divergent social strategies in Pseudomonas aeruginosa populations

Transposable temperate phages randomly insert into bacterial genomes, providing increased supply and altered spectra of mutations available to selection, thus opening alternative evolutionary trajectories. Transposable phages accelerate bacterial adaptation to new environments, but their effect on adaptation to the social environment is unclear. Here we show, using experimental evolution of Pseudomonas aeruginosa in iron-limited and iron-rich environments causing differential expression of siderophore cooperation, that transposable phages promoted divergence into extreme siderophore production phenotypes in iron-limited populations. Iron-limited populations with transposable phages evolved siderophore over-producing clones alongside siderophore non-producing cheats. Low siderophore production was associated with parallel mutations in pvd genes, encoding pyoverdine biosynthesis, and pqs genes, encoding quinolone signaling, while high siderophore production was associated with parallel mutations in phenazine-associated gene clusters. Notably, some of these parallel mutations were caused by phage insertional inactivation. These data suggest that transposable phages, which are widespread in microbial communities, can mediate the evolutionary divergence of social strategies.

evolutionary biology↗

Genetic architecture constrains exploitation of siderophore cooperation in Burkholderia cenocepacia

Explaining how cooperation can persist in the presence of cheaters, exploiting the cooperative acts, is a challenge for evolutionary biology. While microbial systems have proved extremely useful to test evolutionary theory and identify mechanisms maintaining cooperation, our knowledge is often limited to insights gained from a few model organisms. Here, we introduce siderophore secretion by the bacterium Burkholderia cenocepacia as a novel study system. Using a combination of phenotypic and competition assays we found that ornibactin, the main siderophore used for iron scavenging in this species, is secreted into the media, can be shared as public good between cells, but cannot be exploited by ornibactin-defective mutants. Molecular analysis revealed that cheating is compromised because the ornibactin receptor gene and genes involved in ornibactin synthesis are co-expressed from the same operon, such that disruptive mutations in the upstream synthesis genes compromise receptor availability. To prove that it is the genetic architecture of the siderophore locus that prevents cheating, we broke the linked traits by expressing the ornibactin receptor from a plasmid, a measure that turned the ornibactin mutant into a functional cheater. A literature survey across Burkholderia species suggests that the genetic linkage independently broke over evolutionary time scales in several lineages, indicating that cheating and countermeasures might be under selection. Altogether, our results highlight that expanding our repertoire of microbial study systems leads to new discoveries and reinforce the view that social interactions shape evolutionary dynamics in microbial communities.

evolutionary biology↗

Division of labor during biofilm matrix production

Organisms as simple as bacteria can engage in complex collective actions, such as group motility and fruiting body formation. Some of these actions involve a division of labor, where phenotypically specialized clonal subpopulations, or genetically distinct lineages cooperate with each other by performing complementary tasks. Here, we combine experimental and computational approaches to investigate potential benefits arising from division of labor during biofilm matrix production. We show that both phenotypic and genetic strategies for a division of labor can promote collective biofilm formation in the soil bacterium Bacillus subtilis. In this species, biofilm matrix consists of two major components; EPS and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS-producers, and generalists, which produce both EPS and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPS and TasA. The relative fitness of the two mutants displayed a negative frequency dependence both in vitro and on plant roots, with strain frequency reaching a stable equilibrium at 30% TasA-producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modelling, we show that asymmetries in strain ratio can arise due to differences in the relative benefits that matrix compounds generate for the collective; and that genetic division of labor can be favored when it breaks metabolic constraints associated with the simultaneous production of two matrix components.\n\nHighlights- matrix components EPS and TasA are costly public goods in B. subtilis biofilms\n\n- genetic division of labor using {Delta}eps and {Delta}tasA fosters maximal biofilm productivity\n\n- {Delta}eps and {Delta}tasA cooperation is evolutionary stable in laboratory and ecological systems\n\n- costly metabolic coupling of public goods favors genetic division of labor

microbiology↗

The physical boundaries of public goods cooperation between surface-attached bacterial cells

Bacteria secrete a variety of compounds important for nutrient scavenging, competition mediation and infection establishment. While there is a general consensus that secreted compounds can be shared and therefore have social consequences for the bacterial collective, we know little about the physical limits of such bacterial social interactions. Here, we address this issue by studying the sharing of iron-scavenging siderophores between surface-attached microcolonies of the bacterium Pseudomonas aeruginosa. Using single-cell fluorescent microscopy, we show that siderophores, secreted by producers, quickly reach non-producers within a range of 100 m, and significantly boost their fitness. Producers in turn respond to variation in sharing efficiency by adjusting their pyoverdine investment levels. These social effects wane with larger cell-to-cell distances and on hard surfaces. Thus, our findings reveal the boundaries of compound sharing, and show that sharing is particularly relevant between nearby yet physically separated bacteria on soft surfaces, matching realistic natural conditions such as those encountered in soft tissue infections.

evolutionary biology↗