mission pour les initiatives transverses et
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February 15th, 2021 christopher.lefevre@cea.fr
Mission pour les initiatives transverses et interdisciplinaires – MITI
JOURNÉES DE RESTITUTION DU DÉFI ADAPTATION DU VIVANT
SymbioAdapt
Symbioses magnétotactiques: une adaptation des eucaryotes microbiens aux environnements anoxiques
Christopher Lefevre
Bioscience and Biotechnology Institute of Aix-Marseille, CEA Cadarache
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THE MICROBIOMIN GROUP
5 PIs (2 HDR), 3 technical and engineering support
3 post-doctoral associates6 doctoral students
Process whereby microorganisms sequester diverse chemical elements into relatively stable
solid phases called biominerals.
Microbial Bio-Mineralization
What is the biodiversity of biomineralizing microorganisms and that of their biominerals?
What is the evolution and adaptive history of biomineralization processes?
What are their roles in biogeochemical cycles and global change?
What are the chemical pathways and molecular mechanismsof biomineral formation?
FUNDAMENTAL RESEARCH QUESTIONS
TOWARD APPLIED RESEARCH
How can magnetotactic bacteria and magnetic materials be exploited in biotechnologies?
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How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
CEA researcherCaroline Monteil
CNRS researcherChristopher Lefevre
CEA engineerBéatrice Alonso
CEA PhDFrançois Mathon
Sorbonne University PhDCécile Bidaud
CNRS PhDRomain Bolzoni
CEA PhDCamille Mangin
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• Several magnetosomes create a dipolar magnetic moment
• The cell is subjected to a torque and get parallel to the geomagnetic field
• Passive alignment/active motion
0.5 µm0.5 µm
Transmission electron microscopyTransmission electron microscopy
0.5 µm
Transmission electron microscopy
Monteil and Lefèvre (2019) Trends in Microbiology
FreshwaterFreshwater
Marine environmentsMarine environments
Freshwater
Marine environments
Where (Oxic anoxic boundaries) What (magnetotactic organisms)
How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
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Monteil and Lefèvre (2019) Trends in Microbiology
FreshwaterFreshwater
Marine environmentsMarine environments
Freshwater
Marine environments
Where (Oxic anoxix boundaries) What (magnetotactic organisms)
How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
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• Ubiquitous and yet, unknown impact on ecosystem dynamics
• Poorly known diversity and evolutionary histories
• Biological innovations with high technological value
0.5 µm0.5 µm
Transmission electron microscopyTransmission electron microscopy
0.5 µm
Transmission electron microscopy
Monteil and Lefèvre (2019) Trends in Microbiology
FreshwaterFreshwater
Marine environmentsMarine environments
Freshwater
Marine environments
Where (Oxic anoxic boundaries) Why (magnetotactic organisms)
How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
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• Sampling / Magnetic sorting
• Single-cell sorting using micromanipulation
• Transmission electron microscopy and ultramicrotomy
• Single-cell genomics / Taxonomy / Functional annotation
Constraints
Development of single cell characterization
• Organisms recalcitrant to cultivation, requires chemical gradients
How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
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Recent breakthrough: Symbiose magnetotactic
Transmission electron microscopy
Mutualistic symbiosis observed in marine anoxic sediments betweenexcavate protists (Symbiontida, Euglenozoa) and ectosymbioticDeltaproteobacteria biomineralizing ferrimagnetic nanoparticles.
Multi-layered mutualism based on collective magnetotactic motilitywith division of labour and interspecies hydrogen-transfer-basedsyntrophy.
The guided motility of the consortia along the geomagnetic field isallowed by the magnetic moment of the non-motile ectosymbioticbacteria combined with the protist motor activity, which is a uniqueexample of eukaryotic magnetoreception acquired by symbiosis.
Monteil et al (2019) Nature Microbiology
How to assess the biodiversity of magnetotactic microorganisms and that of their biominerals?
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SymbioAdapt – Symbioses magnétotactiques: une adaptation des eucaryotes microbiens aux environnements anoxiques
CNRS Research director
K. Benzerara
SU Professor
N. Menguy
CNRS Research director
G. Perrière
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Institut de minéralogie, de physique des matériaux et de cosmochimie
Bioscience and biotechnology institute of Aix-Marseille
Laboratoire de biométrie et biologie évolutive
INSB INP INEE
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La diversité spécifique des holobiontes par des approches d’écologie microbiennes indépendantes dela culture alliant tri cellulaire par micromanipulation, barcoding et approches de phylogéniemoléculaire.
La physiologie des partenaires sera inférée par l’annotation fonctionnelle de génomes et la génomiquecomparative.
L’évolution de l’interaction sera inférée par génomique évolutive.
Ces approches sont combinées à des approches de chimie, physique des matériaux et minéralogie La structure cellulaire et leur composition chimique seront déterminées par des techniques d’imagerie
impliquant microscopie de haute résolution et spectrométrie des rayons X. Les caractéristiques abiotiques de l’environnement seront déterminées par des approches de
biophysique et géochimie.
SymbioAdaptHypothèse principale: la coopération des sens de chimiotaxie et magnétoréception est répandue chez les eucaryotesunicellulaires et a émergé plusieurs fois dans leur histoire évolutive pour optimiser le déplacement de ces organismesvers les sédiments anoxiques.
Objectifs: ce projet vise à caractériser la biodiversité des holobiontes magnétotactiques et leur environnement,déterminer la biologie cellulaire des partenaires et inférer l’histoire évolutive de leur interaction.
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SymbioAdapt
Main results: 15 morphotypes under characterization
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SymbioAdapt
Main results: 15 morphotypes under characterization
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always found
with MMPs- Length ⁓10 µm
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Light microscope images
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always
found with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts
2 µm
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SEM images
TEM images
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always
found with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protist
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TEM images of thin-sections
1 µm
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always
found with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protist
Protist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and
calcium
2 µmSTEM-Energy-dispersive X-ray spectroscopyelemental maps
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Ca P
Fe S
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always found
with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protist
Protist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and
calcium- Dinoflagellate
Ectosymbionts:- Rod-shaped bacteria that produce bullet-shaped
magnetite and/or greigite magnetosomes
St Rapahaël Carry
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0.5 µm
500 nm
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always found
with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protist
Protist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and
calcium- Dinoflagellate
Ectosymbionts:- Rod-shaped bacteria that produce bullet-shaped
magnetite and/or greigite magnetosomes- Belong to the Desulfobacteraceae, closely related to BW-1
TEM
Symbioticbacteria frommorphotype 4
1816S rRNA phylogenetic tree (draft)
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always found
with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protist
Protist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and
calcium- Dinoflagellate
Ectosymbionts:- Rod-shaped bacteria that produce bullet-shaped
magnetite and/or greigite magnetosomes- Belong to the Desulfobacteraceae, closely related to BW-1
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Transmission
DAPI
EUBp
Desulofacteraceaep
FISH using a flurorescent probe specific to the Desulfobacteraceae family
Magnetotactic holobionts: morphotype 4
Specificities of morphotype 4
Holobiont:- North seeking in the Northern Hemisphere always found
with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external
membrane of the protistProtist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and
calcium- Dinoflagellate
Ectosymbionts:- Rod-shaped bacteria that produce bullet-shaped
magnetite and/or greigite magnetosomes- Belong to the Desulfobacteraceae, closely related to BW-1- Genome sequenced
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Genome 6,7 Mb
Completion 84,7%
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SymbioAdapt: Objectives for 2021
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- Convergent evolution at the origin of the magnetotactic holobionts diversity
- Diversity of magnetotactic symbioses shed light onto the evolutionary step of organellogenesis
- Symbiotic magnetosomes-forming bacteria optimized magnetic moment of their eukaryotic host
SymbioAdapt: Objectives for 2021
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Thanks for your attention
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