Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

Anna Dragoš, Marivic Martin, Carolina Falcón Garcia, Lara Kricks, Patrick Pausch, Thomas Heimerl, Balázs Bálint, Gergely Maróti, Gert Bange, Daniel López, Oliver Lieleg, Ákos T. Kovács*

*Corresponding author for this work

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Abstract

Closely related microorganisms often cooperate, but the prevalence and stability of cooperation between different genotypes remain debatable. Here, we track the evolution of pellicle biofilms formed through genetic division of labour and ask whether partially deficient partners can evolve autonomy. Pellicles of Bacillus subtilis rely on an extracellular matrix composed of exopolysaccharide (EPS) and the fibre protein TasA. In monocultures, ∆eps and ∆tasA mutants fail to form pellicles, but, facilitated by cooperation, they succeed in co-culture. Interestingly, cooperation collapses on an evolutionary timescale and ∆tasA gradually outcompetes its partner ∆eps. Pellicle formation can evolve independently from division of labour in ∆eps and ∆tasA monocultures, by selection acting on the residual matrix component, TasA or EPS, respectively. Using a set of interdisciplinary tools, we unravel that the TasA producer (∆eps) evolves via an unconventional but reproducible substitution in TasA that modulates the biochemical properties of the protein. Conversely, the EPS producer (ΔtasA) undergoes genetically variable adaptations, all leading to enhanced EPS secretion and biofilms with different biomechanical properties. Finally, we revisit the collapse of division of labour between Δeps and ΔtasA in light of a strong frequency versus exploitability trade-off that manifested in the solitarily evolving partners. We propose that such trade-off differences may represent an additional barrier to evolution of division of labour between genetically distinct microorganisms.

Original languageEnglish
JournalNature Microbiology
Volume3
Pages (from-to)1451-1460
ISSN2058-5276
DOIs
Publication statusPublished - 2018

Cite this

Dragoš, Anna ; Martin, Marivic ; Garcia, Carolina Falcón ; Kricks, Lara ; Pausch, Patrick ; Heimerl, Thomas ; Bálint, Balázs ; Maróti, Gergely ; Bange, Gert ; López, Daniel ; Lieleg, Oliver ; Kovács, Ákos T. / Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms. In: Nature Microbiology. 2018 ; Vol. 3. pp. 1451-1460.
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title = "Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms",
abstract = "Closely related microorganisms often cooperate, but the prevalence and stability of cooperation between different genotypes remain debatable. Here, we track the evolution of pellicle biofilms formed through genetic division of labour and ask whether partially deficient partners can evolve autonomy. Pellicles of Bacillus subtilis rely on an extracellular matrix composed of exopolysaccharide (EPS) and the fibre protein TasA. In monocultures, ∆eps and ∆tasA mutants fail to form pellicles, but, facilitated by cooperation, they succeed in co-culture. Interestingly, cooperation collapses on an evolutionary timescale and ∆tasA gradually outcompetes its partner ∆eps. Pellicle formation can evolve independently from division of labour in ∆eps and ∆tasA monocultures, by selection acting on the residual matrix component, TasA or EPS, respectively. Using a set of interdisciplinary tools, we unravel that the TasA producer (∆eps) evolves via an unconventional but reproducible substitution in TasA that modulates the biochemical properties of the protein. Conversely, the EPS producer (ΔtasA) undergoes genetically variable adaptations, all leading to enhanced EPS secretion and biofilms with different biomechanical properties. Finally, we revisit the collapse of division of labour between Δeps and ΔtasA in light of a strong frequency versus exploitability trade-off that manifested in the solitarily evolving partners. We propose that such trade-off differences may represent an additional barrier to evolution of division of labour between genetically distinct microorganisms.",
author = "Anna Dragoš and Marivic Martin and Garcia, {Carolina Falc{\'o}n} and Lara Kricks and Patrick Pausch and Thomas Heimerl and Bal{\'a}zs B{\'a}lint and Gergely Mar{\'o}ti and Gert Bange and Daniel L{\'o}pez and Oliver Lieleg and Kov{\'a}cs, {{\'A}kos T.}",
year = "2018",
doi = "10.1038/s41564-018-0263-y",
language = "English",
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Dragoš, A, Martin, M, Garcia, CF, Kricks, L, Pausch, P, Heimerl, T, Bálint, B, Maróti, G, Bange, G, López, D, Lieleg, O & Kovács, ÁT 2018, 'Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms', Nature Microbiology, vol. 3, pp. 1451-1460. https://doi.org/10.1038/s41564-018-0263-y

Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms. / Dragoš, Anna; Martin, Marivic; Garcia, Carolina Falcón; Kricks, Lara; Pausch, Patrick; Heimerl, Thomas; Bálint, Balázs; Maróti, Gergely; Bange, Gert; López, Daniel; Lieleg, Oliver; Kovács, Ákos T.

In: Nature Microbiology, Vol. 3, 2018, p. 1451-1460.

Research output: Contribution to journalJournal articleResearchpeer-review

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T1 - Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

AU - Dragoš, Anna

AU - Martin, Marivic

AU - Garcia, Carolina Falcón

AU - Kricks, Lara

AU - Pausch, Patrick

AU - Heimerl, Thomas

AU - Bálint, Balázs

AU - Maróti, Gergely

AU - Bange, Gert

AU - López, Daniel

AU - Lieleg, Oliver

AU - Kovács, Ákos T.

PY - 2018

Y1 - 2018

N2 - Closely related microorganisms often cooperate, but the prevalence and stability of cooperation between different genotypes remain debatable. Here, we track the evolution of pellicle biofilms formed through genetic division of labour and ask whether partially deficient partners can evolve autonomy. Pellicles of Bacillus subtilis rely on an extracellular matrix composed of exopolysaccharide (EPS) and the fibre protein TasA. In monocultures, ∆eps and ∆tasA mutants fail to form pellicles, but, facilitated by cooperation, they succeed in co-culture. Interestingly, cooperation collapses on an evolutionary timescale and ∆tasA gradually outcompetes its partner ∆eps. Pellicle formation can evolve independently from division of labour in ∆eps and ∆tasA monocultures, by selection acting on the residual matrix component, TasA or EPS, respectively. Using a set of interdisciplinary tools, we unravel that the TasA producer (∆eps) evolves via an unconventional but reproducible substitution in TasA that modulates the biochemical properties of the protein. Conversely, the EPS producer (ΔtasA) undergoes genetically variable adaptations, all leading to enhanced EPS secretion and biofilms with different biomechanical properties. Finally, we revisit the collapse of division of labour between Δeps and ΔtasA in light of a strong frequency versus exploitability trade-off that manifested in the solitarily evolving partners. We propose that such trade-off differences may represent an additional barrier to evolution of division of labour between genetically distinct microorganisms.

AB - Closely related microorganisms often cooperate, but the prevalence and stability of cooperation between different genotypes remain debatable. Here, we track the evolution of pellicle biofilms formed through genetic division of labour and ask whether partially deficient partners can evolve autonomy. Pellicles of Bacillus subtilis rely on an extracellular matrix composed of exopolysaccharide (EPS) and the fibre protein TasA. In monocultures, ∆eps and ∆tasA mutants fail to form pellicles, but, facilitated by cooperation, they succeed in co-culture. Interestingly, cooperation collapses on an evolutionary timescale and ∆tasA gradually outcompetes its partner ∆eps. Pellicle formation can evolve independently from division of labour in ∆eps and ∆tasA monocultures, by selection acting on the residual matrix component, TasA or EPS, respectively. Using a set of interdisciplinary tools, we unravel that the TasA producer (∆eps) evolves via an unconventional but reproducible substitution in TasA that modulates the biochemical properties of the protein. Conversely, the EPS producer (ΔtasA) undergoes genetically variable adaptations, all leading to enhanced EPS secretion and biofilms with different biomechanical properties. Finally, we revisit the collapse of division of labour between Δeps and ΔtasA in light of a strong frequency versus exploitability trade-off that manifested in the solitarily evolving partners. We propose that such trade-off differences may represent an additional barrier to evolution of division of labour between genetically distinct microorganisms.

U2 - 10.1038/s41564-018-0263-y

DO - 10.1038/s41564-018-0263-y

M3 - Journal article

VL - 3

SP - 1451

EP - 1460

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

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