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Massive gene flux in bacterial population fuels adaptation to forest soil ecosystem

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HAL Id: hal-02314235

https://hal.univ-lorraine.fr/hal-02314235

Submitted on 11 Oct 2019

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Massive gene flux in bacterial population fuels adaptation to forest soil ecosystem

Abdoul-Razak Tidjani, Jean-Noël Lorenzi, Olivier Lespinet, Cyril Bontemps, Pierre Leblond

To cite this version:

Abdoul-Razak Tidjani, Jean-Noël Lorenzi, Olivier Lespinet, Cyril Bontemps, Pierre Leblond. Massive gene flux in bacterial population fuels adaptation to forest soil ecosystem. 15ème congrès de la Société Française de Microbiologie, Sep 2019, Paris 19ème, France. 2019. �hal-02314235�

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Massive gene flux in bacterial population fuels adaptation to forest soil ecosystem

Abdoul-Razak TIDJANI1, Jean-Noël LORENZI1/2, Olivier LESPINET2, Cyril BONTEMPS1, Pierre LEBLOND1

1Université de Lorraine, Inra, DynAMic, F-54000 Nancy, France, 2Institut de Biologie Intégrative de la Cellule (I2BC), CEA, CNRS, Université Paris-Sud, UPSay, Gif-sur-Yvette cedex, France

Introduction

S1A 1 2 3 4 S1B S1C S1D 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 5 6 7 8 0 S1 RLC 1-6 RLB 1-4 S2 S2A 1 2 3 4 S2B S2C S2D 1 2 3 4 1 2 3 4 1 2 3 4 RPA 1-4 RLD 1-4 S3 1-4 RLA 1-4 RPB 1-4 0 2 4 6 8 7 5 3 1 1 2 3 4 5 6 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 1 cm

1. Sampling scheme: To isolate a Streptomyces

population we minimized the spatial scale by performing a micro-scale sampling (from grains of soil)

2. Phylogenetic analyses were then performed to

select strains belonging to the same species (e.g. identical strains in 16S rDNA )

S1A1_18 S1A1_16 S1A1_8 S1A1_3 RLB3_17 S2A2_30 S2A2_7 S1D4_23 S1D4_20 S1D4_18 S1D4_17 S1D4_14 S1D4_10 S1A1_19 S1A1_12 S1A1_7 RPA4_6 RPA4_4 RPA4_3 RLB3-15 RLB3_12 RLB3_6 RLB3_5 RLB1_17 RLB1_16 RLB1_10 RLB1_9 RLB1_8 RLB_7 RLA2_35 RLA_12 RLA2_11 RLA2_9 RLA2_5 S1A1_9 S1D4_5 S1D4_13 94 98 RLB3_4 RLB3_3 100 RPA4_2 S1D4_11 RPA4_30 RLB1_33 RLB1_32 RLB1_30 RLA2_32 100 RPA4_5 RLA4_6 RLA2_7 100 0.002

They are among the biggest bacterial genomes ever sequenced

(ranging from 11.7 to 12.4 Mb)

Phylogenomic analyses confirmed that the strains are closely related at the intra-specific level and derived from a recent common ancestor

 Genome diversity impacts secondary metabolism among closely related

strains.

 Specific metabolites produced by variable genes could serve as public goods

in inhibiting competitors but not other population members.

[1]Hao W., Golding G. B., (2006). The fate of laterally transferred genes: life in the fast lane to adaptation or death. Genome research, 16(5), 636-43.

[2]Wielgoss S., Didelot X., Chaudhuri R.R. et al. (2016); A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. The Isme Journal. 1-10. [3]Vetsigian K., Jajoo R., and Kishony R., (2011). Structure and Evolution of Streptomyces Interaction Networksin Soil and In Silico. PLoS Biol 9 (10): e1001184. doi:10.1371/journal.pbio.1001184.

Strategy

The 11 sequenced genomes were compared with one reference chosen among the population (here RLB1_8). Each bar represents a strain chromosome. Triangles above a chromosome represent an insertion of genes in the reference strain and those below, an insertion in the compared strain. The size of the triangle is proportional to the number of genes in the indel. The highlighted triangles show examples of diversity hotspots where different type of indels are present in the population.

452 indel events (triangles)

ranging from 1 to 241

genes were identified in the population

 Two strains can differ

from 2 to 261 indel events

revealing a great diversity in the population

 There is a gradient of

indel events toward the chromosomal ends

 Some hotspots of

diversity have been

identified (coloured triangles)

 Many positions have

mobile (conjugative) genetic element

signatures, indicating that gene transfers can be the motor of the diversity

Comparison of a diversity hotspot between 3 strains.

The white boxes represent strain specific indels and grey boxes conserved regions. Brown and purple boxes represent gene clusters involved in secondary metabolite synthesis.

The bioassay shows that only RLB1-9 can inhibit the growth of a Bacillus indicator strain.

Mutation of the RLB1-9 NRPS showed that it was responsible of the Bacillus inhibition.

Strains of the population do not inhibit each other in same conditions (data not shown).

 This study revealed an unexpectedly genetic diversity in term of presence/absence of genes among a Streptomyces population.

 Massive gene fluxes can explain how such diversification can occur within short evolutionary time.

 The diversity observed between individuals can have a functional role and impacts the ecology of the whole population.

This work was supported by Labex ARBRE

16S rDNA phylogenetic tree

Strains in each coloured clade have identical 16S rDNA sequences.

Strains in red in the purple clade were chosen to be sequenced

3. The genomes of 11 strains of the population were sequenced and

compared.

The genomes are organized as linear chromosomes, some of them bearing large extrachromosomal elements

Pairwise comparisons of genomes were performed to identify variable gene pools due to insertion or deletion events (indels)

The strains of a population are not necessarily clones and some can have specific genes that are not shared by all of the individuals of the

population[1,2]. The real extent of this population genome variation in soil bacteria remains poorly described.

We aimed here to decipher by genome comparison the proportion of the specific genes, the mechanisms shaping these variations and their potential roles in a Streptomyces population.

Streptomyces are soil dwelling bacteria. They have a linear chromosome and a prolific specialized metabolism (e.g. enzymes, antibiotics,

antifungals…) often of high biotechnological and medical interests. They can play key roles in the plant rhizosphere by contributing to their growth, health and resilience.

As for plant or animal, bacteria are naturally structured in populations, i.e. individuals of the same species that interact together in the same environment.

cm

A large number of indels exists between the different strains of the population

Conclusions

The population genetic diversity can have ecological impacts

Exemple of grains sampled from soil

Bacillus

Streptomyces

Genomic diversity hotspot Bioassay

BGC (33 CDS): 40.6kb 90 kb Nucleoside-NRPS (40 CDS): 56.6 kb 10 kb RLB1-9 RLB1-8 RLB3-17 220 kb RLB1-8 RLB3-5 S1d4-20 S1d4-14 S1A1-7 S1A1-3 S1A1-8 RLB1-9 RLB3-17 S1d4-23 RLB3-6

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