Experimental Evolution as an Underutilized Tool for Studying Beneficial Animal–Microbe Interactions

Rapid evolution of bacterial mutualism in the plant rhizosphere

10.1101/2020.12.07.414607 ◽

2020 ◽

Author(s):

Erqin Li ◽

Ronnie de Jonge ◽

Chen Liu ◽

Henan Jiang ◽

Ville-Petri Friman ◽

...

Keyword(s):

Experimental Evolution ◽

Direct Evidence ◽

Rapid Evolution ◽

Evolutionary Transition ◽

Transcription Factor Gene ◽

Growth Cycles ◽

Factor Gene ◽

Two Component ◽

Microbe Interactions ◽

Fitness Benefits

SummaryEven 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.

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Rapid evolution of bacterial mutualism in the plant rhizosphere

Nature Communications ◽

10.1038/s41467-021-24005-y ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Erqin Li ◽

Ronnie de Jonge ◽

Chen Liu ◽

Henan Jiang ◽

Ville-Petri Friman ◽

...

Keyword(s):

Plant Growth ◽

Experimental Evolution ◽

Direct Evidence ◽

Rapid Evolution ◽

Evolutionary Transition ◽

Growth Cycles ◽

Two Component ◽

Microbe Interactions ◽

Fitness Benefits ◽

Positive Effect

AbstractWhile beneficial plant-microbe interactions are common in nature, direct evidence for the evolution of bacterial mutualism is scarce. Here we use experimental evolution to causally show that initially plant-antagonistic Pseudomonas protegens bacteria evolve into mutualists in the rhizosphere of Arabidopsis thaliana within six plant growth cycles (6 months). This evolutionary transition is accompanied with increased mutualist fitness via two mechanisms: (i) improved competitiveness for root exudates and (ii) enhanced tolerance to the plant-secreted antimicrobial scopoletin whose production is regulated by transcription factor MYB72. Crucially, these mutualistic adaptations are coupled with reduced phytotoxicity, enhanced transcription of MYB72 in roots, and a positive effect on plant growth. Genetically, mutualism is associated with diverse mutations in the GacS/GacA two-component regulator system, which confers high fitness benefits only in the presence of plants. Together, our results show that rhizosphere bacteria can rapidly evolve along the parasitism-mutualism continuum at an agriculturally relevant evolutionary timescale.

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Experimental evolution of independent genetic pathways for resistance to Pseudomonas aeruginosa pathogenicity within the nematode Caenorhabditis remanei

10.1101/484998 ◽

2018 ◽

Cited By ~ 1

Author(s):

Heather Archer ◽

Patrick C. Phillips

Keyword(s):

Pseudomonas Aeruginosa ◽

Experimental Evolution ◽

Genetic Basis ◽

Opportunistic Pathogen ◽

Nematode Resistance ◽

Genetic Pathways ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

Caenorhabditis Remanei ◽

Pathogenic Effects

ABSTRACTPathogenic host-microbe interactions can result from continuous evolution of a host’s ability to resist infection and a pathogen’s ability to survive and replicate. Pseudomonas aeruginosa is a versatile and opportunistic pathogen, ubiquitous in the environment, and capable of damaging plants, vertebrates, and invertebrates. Previous studies in nematodes suggest that the pathogenic effects of P. aeruginosa can result from multiple distinct pathways: a toxin-based effect that kills within a few hours and a generalized virulence that kills over the course of multiple days. Using experimental evolution in the highly polymorphic nematode Caenorhabditis remanei, we show that nematode resistance to the two modes of pathogenesis in P. aeruginosa evolves through genetically independent pathways. These results demonstrate that multiple virulence patterns in a pathogen can result in multiple responses in the host, and the genetic lines established here create resources for further exploration of the genetic basis for resistance to P. aeruginosa.

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Experimental evolution of a fungal pathogen into a gut symbiont

Science ◽

10.1126/science.aat0537 ◽

2018 ◽

Vol 362 (6414) ◽

pp. 589-595 ◽

Cited By ~ 65

Author(s):

Gloria Hoi Wan Tso ◽

Jose Antonio Reales-Calderon ◽

Alrina Shin Min Tan ◽

XiaoHui Sem ◽

Giang Thi Thu Le ◽

...

Keyword(s):

Experimental Evolution ◽

Fungal Pathogen ◽

Experimental System ◽

New Host ◽

Evolutionary Forces ◽

Cytokine Responses ◽

Microbe Interactions ◽

New Hosts ◽

Opportunistic Fungal Pathogen ◽

Systemic Infections

Gut microbes live in symbiosis with their hosts, but how mutualistic animal-microbe interactions emerge is not understood. By adaptively evolving the opportunistic fungal pathogenCandida albicansin the mouse gastrointestinal tract, we selected strains that not only had lost their main virulence program but also protected their new hosts against a variety of systemic infections. This protection was independent of adaptive immunity, arose as early as a single day postpriming, was dependent on increased innate cytokine responses, and was thus reminiscent of “trained immunity.” Because both the microbe and its new host gain some advantages from their interaction, this experimental system might allow direct study of the evolutionary forces that govern the emergence of mutualism between a mammal and a fungus.

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Virus-host coexistence in phytoplankton through the genomic lens

Science Advances ◽

10.1126/sciadv.aay2587 ◽

2020 ◽

Vol 6 (14) ◽

pp. eaay2587 ◽

Cited By ~ 5

Author(s):

Sheree Yau ◽

Marc Krasovec ◽

L. Felipe Benites ◽

Stephane Rombauts ◽

Mathieu Groussin ◽

...

Keyword(s):

Experimental Evolution ◽

Large Deletion ◽

Genomic Rearrangements ◽

Dsdna Virus ◽

Viral Production ◽

Boom And Bust ◽

Microbe Interactions ◽

Clonal Lines ◽

Virus Interactions ◽

Parallel Growth

Virus-microbe interactions in the ocean are commonly described by “boom and bust” dynamics, whereby a numerically dominant microorganism is lysed and replaced by a virus-resistant one. Here, we isolated a microalga strain and its infective dsDNA virus whose dynamics are characterized instead by parallel growth of both the microalga and the virus. Experimental evolution of clonal lines revealed that this viral production originates from the lysis of a minority of virus-susceptible cells, which are regenerated from resistant cells. Whole-genome sequencing demonstrated that this resistant-susceptible switch involved a large deletion on one chromosome. Mathematical modeling explained how the switch maintains stable microalga-virus population dynamics consistent with their observed growth pattern. Comparative genomics confirmed an ancient origin of this “accordion” chromosome despite a lack of sequence conservation. Together, our results show how dynamic genomic rearrangements may account for a previously overlooked coexistence mechanism in microalgae-virus interactions.

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Neurotropic enteroviruses co-opt “fair-weather-friend” commensal gut microbiota to drive host infection and central nervous system disturbances

Behavioral and Brain Sciences ◽

10.1017/s0140525x18002741 ◽

2019 ◽

Vol 42 ◽

Author(s):

Kevin B. Clark

Keyword(s):

Central Nervous System ◽

Nervous System ◽

Gut Bacteria ◽

Infection Cycle ◽

Fair Weather ◽

Host Health ◽

Microbe Interactions ◽

Animal Hosts ◽

Host Infection ◽

Neuropsychiatric Conditions

Abstract Some neurotropic enteroviruses hijack Trojan horse/raft commensal gut bacteria to render devastating biomimicking cryptic attacks on human/animal hosts. Such virus-microbe interactions manipulate hosts’ gut-brain axes with accompanying infection-cycle-optimizing central nervous system (CNS) disturbances, including severe neurodevelopmental, neuromotor, and neuropsychiatric conditions. Co-opted bacteria thus indirectly influence host health, development, behavior, and mind as possible “fair-weather-friend” symbionts, switching from commensal to context-dependent pathogen-like strategies benefiting gut-bacteria fitness.

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