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Friman, V.-P.

Publications and source records attributed to Friman, V.-P..

10 recordsLinked to original sources

Eco-evolutionary dynamics and environmental detoxification jointly shape bacterial community response to antibiotic perturbation

Microbial communities frequently encounter recurrent antibiotic disturbance, yet how ecological, evolutionary, and environmental processes jointly shape the response remains unresolved. Here we experimentally disentangle these mechanisms using a 23-species bacterial community exposed to ampicillin pulses with pre-pulse and resistance priming. Pre-pulse priming preconditioned community composition toward resistant taxa, reducing compositional change during the main pulse. Resistance priming was the dominant determinant of community response, buffering compositional change, relaxing selection, and altering gene expression. This buffering arose from both evolution of higher resistance and accelerated ampicillin detoxification by a dominant degrader, which transiently reduced antibiotic effects and favoured non-degrading taxa. Yet buffering did not translate into better recovery: because resistance was coupled to competitive dominance, diversity remained comparable to or below that of ancestral communities, and dominance was reinforced. Together, we show that antibiotic history reshapes microbial disturbance response through coupled eco-evolutionary and environmental feedbacks, generating a trade-off between resistance and recovery.

evolutionary biology↗

From sequence to ecology: siderophore-receptor coevolution algorithm predicts bacterial interactions in complex communities

Predicting bacterial social interactions from genome sequences is notoriously difficult. Here, we developed bioinformatic tools to predict whether secreted iron-scavenging siderophores stimulate or inhibit the growth of community members. Siderophores are chemically diverse and can be stimulatory or inhibitory depending on whether bacteria possess or lack corresponding uptake receptors. We focused on 1928 representative Pseudomonas genomes and developed a co-evolution algorithm to match all encoded siderophore synthetases to corresponding receptor gene groups with >90% accuracy based on experimental validation. We derived community-level iron interaction networks to show that selection for siderophore-mediated interactions differs across habitats and lifestyles. Specifically, dense networks of siderophore sharing and competition were observed among environmental (soil/water/plant) strains and non-pathogenic species, while only fragmented networks occurred among human-derived strains and pathogenic species. Altogether, our sequence-to-ecology approach empowers the analyses of social interactions among thousands of bacterial strains and uncovers ways for targeted intervention to microbial communities. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=87 SRC="FIGDIR/small/565711v3_ufig1.gif" ALT="Figure 1"> View larger version (22K): org.highwire.dtl.DTLVardef@60d907org.highwire.dtl.DTLVardef@48756eorg.highwire.dtl.DTLVardef@115aac1org.highwire.dtl.DTLVardef@17d76e5_HPS_FORMAT_FIGEXP M_FIG C_FIG

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↗

Influence of insertion sequences on population structure of phytopathogenic bacteria in the Ralstonia solanacearum species complex

Ralstonia solanacearum species complex (RSSC) is a destructive group of plant pathogenic bacteria and the causative agent of bacterial wilt disease. Experimental studies have attributed RSSC virulence to insertion sequences (IS), transposable genetic elements which can both disrupt and activate host genes. Yet, the global diversity and distribution of RSSC IS are unknown. In this study, IS were bioinformatically identified in a diverse collection of 356 RSSC strains representing four phylogenetic lineages, and their diversity investigated based on genetic distance measures and comparisons with the ISFinder database. IS distributions were characterised using metadata on RSSC lineage classification and potential gene disruptions by IS were determined based on their proximity to coding sequences. In total, we found 24,732 IS belonging to eleven IS families and 26 IS subgroups, with over half of the IS found in the megaplasmid. While IS families were generally widespread across the RSSC phylogeny, IS subgroups showed strong lineage-specific distributions and genetically similar bacterial strains had similar IS contents. Further, IS present in multiple lineages were generally found in different genomic regions suggesting potential recent horizontal transfer. Finally, IS were found to disrupt many genes with predicted functions in virulence, stress tolerance, and metabolism, suggesting that they might be adaptive. This study highlights that RSSC insertion sequences track the evolution of their bacterial hosts, potentially contributing to both intra- and inter-lineage genetic diversity.

genomics↗

The effects of antibiotic combination treatments on Pseudomonas aeruginosa tolerance evolution and coexistence with Stenotrophomonas maltophilia

Pseudomonas aeruginosa bacterium is a common pathogen of Cystic Fibrosis (CF) patients due to its ability to evolve resistance to antibiotics during treatments. While P. aeruginosa resistance evolution is well characterised in monocultures, it is less well understood in polymicrobial CF infections. Here, we investigated how exposure to ciprofloxacin, colistin, or tobramycin antibiotics, administered at sub-MIC doses alone and in combination, shaped the tolerance evolution of P. aeruginosa (PAO1 lab and clinical CF LESB58 strains) in the absence and presence of a commonly co-occurring species, Stenotrophomonas maltophilia. Increases in antibiotic tolerances were primarily driven by the presence of that antibiotic in the treatment. We observed a reciprocal cross-tolerance between ciprofloxacin and tobramycin, and when combined these antibiotics selected increased MICs for all antibiotics. Though the presence of S. maltophilia did not affect the tolerance or the MIC evolution, it drove P. aeruginosa into extinction more frequently in the presence of tobramycin due to its relatively greater innate tobramycin tolerance. In contrast, P. aeruginosa dominated and drove S. maltophilia extinct in most other treatments. Together, our findings suggest that besides driving high-level antibiotic tolerance evolution, sub-MIC antibiotic exposure can alter competitive bacterial interactions, leading to target pathogen extinctions in multi-species communities.

microbiology↗

Engineering ecologically complementary rhizosphere probiotics using consortia of specialized bacterial mutants

While bacterial diversity is beneficial for the functioning of rhizosphere microbiomes, multi-species bioinoculants often fail to promote plant growth. One potential reason for this is that competition between inoculated consortia members create conflicts for their survival and functioning. To circumvent this, we used transposon mutagenesis to increase the functional diversity within Bacillus amyloliquefaciens bacterial species and tested if we could improve plant growth-promotion by assembling consortia of closely related but functionally specialized mutants. While most insertion mutations were harmful, some improved strains plant growth-promotion traits without increasing antagonism between them. Crucially, plant growth-promotion could be improved by applying these specialist mutants as consortia, leading to clear positive relationships between consortia richness, plant root colonization and protection from bacterial wilt disease. Together, our results suggest that increasing intra-species diversity could be an effective way to increase probiotic consortia multifunctionality, leading to more stable plant growth-promotion throughout growth cycle via insurance effects.

ecology↗

Global diversity and distribution of prophages is lineage-specific within the Ralstonia solanacearum plant pathogenic bacterium species complex

Ralstonia solanacearum is a destructive plant pathogenic bacterium and the causative agent of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, its virulence is mediated by mobile genetic elements including integrated DNA of bacteriophages, i.e., prophages, which may carry fitness-associated auxiliary genes or modulate host gene expression. Although experimental studies have characterised several prophages that shape R. solanacearum virulence, the global diversity, distribution, and wider functional gene content of R. solanacearum prophages is unknown. In this study, prophages were identified in a diverse collection of 192 R. solanacearum draft genome assemblies originating from six continents. Prophages were identified bioinformatically and their diversity investigated using genetic distance measures, gene content, GC, and total length. Prophage distribution was characterised using metadata on R. solanacearum geographic origin and lineage classification (phylotypes), and their functional gene content was assessed by identifying putative prophage-encoded auxiliary genes. In total, 343 intact prophages were identified, forming ten genetically distinct clusters. These included five prophage clusters belonging to the Inoviridae, Myoviridae, and Siphoviridae phage families, and five uncharacterised clusters, possibly representing novel, previously undescribed phages. The prophages had broad geographical distribution being present across multiple continents. However, they were generally host phylogenetic lineage-specific, and overall, prophage diversity was proportional to the genetic diversity of their hosts. The prophages contained a myriad of auxiliary genes involved in metabolism and virulence of both phage and bacteria. Our results show that while R. solanacearum prophages are highly diverse globally, they make lineage-specific contributions to the R. solanacearum accessory genome, which could have resulted from shared coevolutionary history.

microbiology↗

Parallel evolution of phage resistance - virulence trade - offs during in vitro and nasal Pseudomonas aeruginosa phage treatment

With rising antibiotic resistance, there has been increasing interest in treating pathogenic bacteria with bacteriophages (phage therapy). One limitation of phage therapy is the ease at which bacteria can evolve resistance. Negative effects of resistance may be mitigated when resistance results in reduced bacterial growth and virulence, or when phage coevolve to overcome resistance. Resistance evolution and its consequences are contingent on the bacteria-phage combination and their environmental context, making therapeutic outcomes hard to predict. One solution might be to conduct "in vitro evolutionary simulations" using bacteria-phage combinations from the therapeutic context. Overall, our aim was to investigate parallels between in vitro experiments and in vivo dynamics in a human participant. Evolutionary dynamics were similar, with high levels of resistance evolving quickly with limited evidence of phage evolution. Resistant bacteria - evolved in vitro and in vivo - had lower virulence. In vivo, this was linked to lower growth rates of resistant isolates, whereas in vitro phage resistant isolates evolved greater biofilm production. Population sequencing suggests resistance resulted from selection on de novo mutations rather than sorting of existing variants. These results highlight the speed at which phage resistance can evolve in vivo, and in vitro experiments may give useful insights for clinical evolutionary outcomes.

evolutionary biology↗

Rapid evolution of bacterial mutualism in the plant rhizosphere

Even though beneficial plant-microbe interactions are commonly observed in nature, direct evidence for the evolution of bacterial mutualism in the rhizosphere remains elusive. Here we use experimental evolution to causally show that initially plant-antagonistic Pseudomonas protegens bacterium evolves into mutualists in the rhizosphere of Arabidopsis thaliana within six plant growth cycles (6 months). This evolutionary transition was accompanied with increased mutualist fitness via two mechanisms: i) improved competitiveness for root exudates and ii) enhanced capacity for activating the root-specific transcription factor gene MYB72, which triggers the production of plant-secreted scopoletin antimicrobial for which the mutualists evolved relatively higher tolerance to. Genetically, mutualism was predominantly associated with different mutations in the GacS/GacA two-component regulator system, which conferred high fitness benefits only in the presence of plants. Together, our results show that bacteria can rapidly evolve along the parasitism-mutualism continuum in the plant rhizosphere at an agriculturally relevant evolutionary timescale.

microbiology↗

MAUI-seq: Multiplexed, high-throughput amplicon diversity profiling using unique molecular identifiers

BackgroundSequencing and PCR errors are a major challenge when characterising genetic diversity using high-throughput amplicon sequencing (HTAS). ResultsWe have developed a multiplexed HTAS method, MAUI-seq, which uses unique molecular identifiers (UMIs) to improve error correction by exploiting variation among sequences associated with a single UMI. We show that two main advantages of this approach are efficient elimination of chimeric and other erroneous reads, outperforming DADA2 and UNOISE3, and the ability to confidently recognise genuine alleles that are present at low abundance or resemble chimeras. ConclusionsThe method provides sensitive and flexible profiling of diversity and is readily adaptable to most HTAS applications, including microbial 16S rRNA profiling and metabarcoding of environmental DNA.

ecology↗