mission pour les initiatives transverses et

February 15th, 2021 [email protected]

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)


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Freshwater

Marine environments

Where (Oxic anoxix boundaries) What (magnetotactic organisms)


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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





Freshwater

Marine environments

Where (Oxic anoxic boundaries) Why (magnetotactic organisms)


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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


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Recent breakthrough: Symbiose magnetotactic


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


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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



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




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




found with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external


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




with MMPs- Length ⁓10 µm- 1 protist with up to 8 ectosymbionts- Bacteria are localized in invaginations of the external



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









magnetite and/or greigite magnetosomes- Belong to the Desulfobacteraceae, closely related to BW-1

TEM

Symbioticbacteria frommorphotype 4

1816S rRNA phylogenetic tree (draft)









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





membrane of the protistProtist:- 2 flagella. One pulling, the other pushing- Biomineralize crystalline particles rich in phosphorus and



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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