Four-Species Pathogen Community Under DMS3vir Phage Predation

An artificial four-species bacterial community — Pseudomonas aeruginosa PA14, Acinetobacter baumannii, Staphylococcus aureus, and Burkholderia cenocepacia — propagated for 10 days in lysogeny broth with and without the lytic phage DMS3vir, which infects P. aeruginosa through its Type IV pilus. Without phage, P. aeruginosa outcompetes the other three species. Adding DMS3vir drives P. aeruginosa nearly extinct and releases A. baumannii into dominance, while maintaining community diversity. The experiment is fully factorial over all 1-, 2-, 3-, and 4-species combinations and over two P. aeruginosa clones (wild type and an isogenic CRISPR-KO), which lets the record separate the community consequences of phage predation from the consequences of which resistance mechanism evolves: the two resistance routes gave largely indistinguishable community dynamics, and surface-based resistance classified by the authors as Type IV pilus mutation became dominant even where CRISPR-Cas was functional. That classification is phenotype-based; the receptor mutants were not sequenced in this study. This is a one-phage-on-many-bacteria (1-N) system in the sense of doi:10.1146/annurev-virology-100424-123645 — a single phage population against a bacterial community — and the record exists to carry the community-level consequences of phage predation rather than the phage-host pair itself. The tested pairwise-fitted generalized Lotka-Volterra models failed to predict the larger community. This supports a context-dependence interpretation without establishing a general impossibility of prediction from pairwise information. Adding three-species data improved quantitative prediction without phage; with phage, quantitative failure remained despite a qualitative competitive-release prediction.

Taxonomy

Taxon Ontology ID Functional Roles Abundance
Pseudomonas aeruginosa PA14 — ontology label: Pseudomonas aeruginosa NCBITaxon:287 · TaxonMech · TraitMech DOMINANT
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "The bacteria P. aeruginosa UCBPP-PA14 strain marked with streptomycin resistance, the PA14 csy3::LacZ strain (CRISPR-KO), and phages DMS3vir and DMS3vir+acrF1 were used throughout this study"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "P. aeruginosa outcompetes the other species in the absence of phage"
Acinetobacter baumannii FZ21 — ontology label: Acinetobacter baumannii NCBITaxon:470 · TaxonMech · TraitMech RARE
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "The microbial community consisted of S. aureus strain 13 S44 S9 and A. baumannii clinical isolate FZ21 which were isolated at Queen Astrid Military Hospital, Brussels, Belgium"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "with A. baumannii reaching particularly high abundance"
Staphylococcus aureus 13 S44 S9 — ontology label: Staphylococcus aureus NCBITaxon:1280 · TaxonMech · TraitMech RARE
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "The microbial community consisted of S. aureus strain 13 S44 S9 and A. baumannii clinical isolate FZ21 which were isolated at Queen Astrid Military Hospital, Brussels, Belgium"
Burkholderia cenocepacia J2315 — ontology label: Burkholderia cenocepacia NCBITaxon:95486 · TaxonMech · TraitMech RARE
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "B. cenocepacia J2315 was originally isolated from a person with cystic fibrosis in the UK in 1989"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "we consistently observed persistence of B. cenocepacia at an average of approximately 104 cfu/ml across all treatments"
Pseudomonas phage DMS3vir — ontology label: Casadabanvirus DMS3 NCBITaxon:389469 · TaxonMech · TraitMech
LYTIC_PHAGE
RARE
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "S. aureus, A. baumannii, B. cenocepacia, and P. aeruginosa PA14 in the presence or absence of lytic phage DMS3vir"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "Phage DMS3vir was added at 106 pfu. prior to inoculation"

Ecological Interactions

The graph shows only explicitly linked interaction participants. Community members without an asserted participant link are omitted; membership alone does not imply an interaction.

Ecological interaction network for Four-Species Pathogen Community Under DMS3vir Phage Predation Bipartite graph where circles represent taxa and non-circular symbols represent interactions. Rare or untyped interactions share the Other symbol; exact curated types remain in the interaction details.
Taxon
Other

DMS3vir Lytic Infection of Pseudomonas aeruginosa via the Type IV Pilus

LYTIC_INFECTION

Phage DMS3vir infects P. aeruginosa PA14 by adsorbing to the Type IV pilus, replicating to high titre on sensitive hosts before host resistance evolves and phage densities collapse. The paper treats DMS3vir as a P. aeruginosa- targeting phage throughout and reports no infection of the other three species; it does not report host-range assays against them, so the absence of other hosts is the study's framing rather than a tested result.

Source Taxon: Pseudomonas phage DMS3vir

Target Taxon: Pseudomonas aeruginosa PA14

Biological Processes:

Downstream Effects:
→ Competitive Release of Acinetobacter baumannii

Lysis of the otherwise dominant competitor is what frees the niche that A. baumannii expands into.

→ Type IV Pilus Mutation Dominates Realised Resistance

PARTIAL: Phage exposure provided the selection context in which surface-based resistance became dominant. This links infection to the observed resistance response, but does not show that receptor targeting itself causes a measured fitness cost or establishes the proposed cost-mediated explanation for continued host non-recovery.

Evidence

  • PMID:38648198 - SUPPORT (IN_VITRO)
    "Phage DMS3vir targets P. aeruginosa’s Type IV pilus (T4P)"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "phage DMS3vir initially reached high titres due to replication on sensitive P. aeruginosa hosts, followed by a rapid decline in phage densities due to the evolution of phage resistance"

Competitive Release of Acinetobacter baumannii

COMPETITIVE_RELEASE

Phage predation removes P. aeruginosa, the strongest competitor, and A. baumannii expands into the vacated niche to become the dominant species. The release occurred in every treatment and did not depend on whether the P. aeruginosa clone had a functional CRISPR-Cas system. Without phage the hierarchy is the reverse, with P. aeruginosa outcompeting all three others.

Participating Taxa: Acinetobacter baumannii FZ21, Pseudomonas aeruginosa PA14

Downstream Effects:
→ Phage-Associated Maintenance of Community Diversity

PARTIAL: Competitive release is a proposed component of the phage-associated community shift and diversity maintenance. Phage addition altered both outcomes, but the experiment does not isolate expansion of A. baumannii alone as a necessary or sufficient mediator of the diversity effect.

Evidence

  • PMID:38648198 - SUPPORT (IN_VITRO)
    "the presence of phage caused microbial communities to no longer be dominated by P. aeruginosa"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "the competitive release of A. baumannii occurred in all treatments and was virtually independent of whether P. aeruginosa had a functional CRISPR-Cas immune system or not"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "P. aeruginosa outcompetes the other species in the absence of phage"

Type IV Pilus Mutation Dominates Realised Resistance

P. aeruginosa can resist DMS3vir either by CRISPR-Cas immunity or by losing or modifying the Type IV pilus receptor. Pilus mutation became the dominant realised mechanism even in clones with a functional CRISPR system, and the associated fitness cost is the proposed reason P. aeruginosa does not recover after the phage is driven extinct. The wild type did reach higher relative abundance than the CRISPR-KO when A. baumannii was present, early on while phage persisted. This node records the observed resistance response and its qualified ecological interpretation; it does not assert reciprocal negative fitness effects between the listed participants. The mutation terminology is the authors' phenotype-based classification of surface-based resistance; these receptor mutants were not sequenced in this study, so it does not establish their specific genotypes.

Participating Taxa: Pseudomonas aeruginosa PA14, Acinetobacter baumannii FZ21

Evidence

  • PMID:38648198 - SUPPORT (IN_VITRO)
    "mutation of the Type IV pilus became the dominant resistance mechanism even if P. aeruginosa has a functional CRISPR system"
  • PMID:38648198 - PARTIAL (IN_VITRO)
    "which might in part be why P. aeruginosa did not recover in the microbial community post phage exposure due to the associated fitness costs"
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "Further sequencing of receptor mutants was not done"

Phage-Associated Maintenance of Community Diversity

Adding phage prevented the extinctions seen in the phage-free treatments: very few or none of the replicates lost a species, and the authors report a diversity-maintaining effect on Shannon diversity over time. This is a community-level treatment outcome, not an additional virus-to-host infection. The actual pairwise infection is represented separately. A single competitive release does not establish the repeated or alternating dominance required by KILL_THE_WINNER; no such interaction type is assigned here.

Evidence

  • PMID:38648198 - SUPPORT (IN_VITRO)
    "very few to none of the experimental repeats had 1 or more bacterial species go extinct"
  • PMID:38648198 - PARTIAL (IN_VITRO)
    "phage targeting a dominant species allows for the competitive release of the strongest competitor while also contributing to community diversity maintenance"

Model-Inferred Context Dependence of Community Interactions

PARTIAL: The tested generalized Lotka-Volterra models fitted to pairwise data failed to predict three- and four-species dynamics, consistent with context-dependent interactions. This diagnostic does not isolate a particular higher-order mechanism or prove that no pairwise-based model could describe the community. Incorporating two- and three-species data improved quantitative four-species prediction in the absence of phage. With phage, the fitted coefficients still failed to generalize quantitatively to four species, although the model captured a qualitative competitive-release shift. The authors identify omitted explicit phage dynamics as a possible structural limitation. These are computational findings, not a new measured reciprocal-competition relation.

Evidence

  • PMID:38648198 - PARTIAL (COMPUTATIONAL)
    "fitting gLV models with pairwise only datasets led to predictive failures when applied to 3- or 4-species datasets"
  • PMID:38648198 - PARTIAL (COMPUTATIONAL)
    "pairwise data alone is insufficient when modelling our microbial community"
  • PMID:38648198 - SUPPORT (COMPUTATIONAL)
    "reasonably fit the data in the absence of phage"
  • PMID:38648198 - SUPPORT (COMPUTATIONAL)
    "the interaction coefficients did not generalise quantitatively to 4-species data"

Knowledge gaps & discussions (4)

CURATION_TODO OPEN Should CommunityMech represent time-resolved composition, or keep trajectories in linked datasets and carry only the qualitative dynamic claim as an interaction?

The curated finding here is a trajectory — P. aeruginosa falls and A. baumannii rises over 10 days — but TaxonomicComposition carries a single abundance per member with no time axis, so `abundance_level` had to be set to the phage-free baseline and the trajectory written into interaction descriptions instead. A consumer reading abundances alone sees P. aeruginosa DOMINANT and A. baumannii RARE, which is the pre-phage state and the opposite of this record's point. What would resolve it is a decision about whether CommunityMech represents time-series composition at all, or deliberately keeps trajectories in linked datasets and carries only the qualitative dynamic claim in `ecological_interactions`. This record is a good test case either way: the underlying per-timepoint densities are published.

Attaches to: taxonomy

OPEN_QUESTION OPEN Does this study establish recurring changes in dominance, beyond the observed single competitive release, sufficient to support KILL_THE_WINNER?

The reported experiment shows one competitive release and subsequent phage decline, not recurring alternation of the dominant species. KILL_THE_WINNER is therefore not assigned. The diversity outcome is also not a separate lytic infection: the direct phage-host relation is already represented by its own pairwise node. This record does not establish what would happen under other time horizons or ecological conditions.

Attaches to: ecological_interactions#Phage-Associated Maintenance of Community Diversity

CURATION_TODO OPEN Where should a phage-resistance mechanism (receptor mutation versus defence system) and its fitness cost be recorded, now that prose in an interaction description is the only option?

The record distinguishes observed resistance-route frequencies from the proposed fitness-cost explanation for non-recovery. No dedicated mechanism or cost slot is used here, but interaction_type is optional: the absence of a more specific type does not justify a COMPETITION label asserting reciprocal negative effects. The observations and their source-qualified interpretation remain in the node description and evidence without that label.

Attaches to: ecological_interactions#Type IV Pilus Mutation Dominates Realised Resistance

KNOWLEDGE_GAP OPEN How much of the phage-associated diversity effect is mediated by competitive release of A. baumannii?

The phage addition comparison supports changes in both dominance and diversity. The inspected Results and Discussion do not isolate the released competitor as a necessary or sufficient cause of diversity maintenance. The existing arrow therefore retains a PARTIAL mediation interpretation rather than a fully resolved mechanistic chain. A direct mediation assessment in this exact community would be needed to strengthen that claim.

Attaches to: ecological_interactions#Competitive Release of Acinetobacter baumannii, ecological_interactions#Phage-Associated Maintenance of Community Diversity

1 evidence item(s)
full_text PARTIAL PMID:38648198

phage targeting a dominant species allows for the competitive release of the strongest competitor while also contributing to community diversity maintenance

The authors summarize competitive release and diversity maintenance as joint phage-associated outcomes; this sentence does not isolate their mediation.

External Resources

Name Repository Resource ID
Primary publication for the four-species phage predation community
PubMed record for Alseth et al. 2024, PLoS Biology, "The impact of phage and phage resistance on microbial community dynamics".
OTHER PMID:38648198
DOI landing page
DOI link to the PLoS Biology paper.
OTHER doi:10.1371/journal.pbio.3002346
Generalised Lotka-Volterra modelling code
Matlab code for the gLV parameterisation and the analysis of phage-dependent competitive release.
GITHUB GaTechBrownLab/phage-community-dynamics
  • PMID:38648198 - SUPPORT (COMPUTATIONAL)
    "All modelling and analysis was done using Matlab 2021b and the code is publicly available at"

Environmental Factors

Factor Value Unit
Temperature 37 degree Celsius
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "the bacterial mixtures were grown at 37°C and shaking at 180 r.p.m."
Serial transfer regime 1:100 every 24 h for 10 days N/A
  • PMID:38648198 - SUPPORT (IN_VITRO)
    "with transfers of 1:100 into fresh LB medium being done every 24 h"

Growth Media

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