Our Research
Wolbachia are the most prevalent endosymbionts on earth, present in a majority of terrestrial arthropods species and in parasitic filarial nematodes. We are interested in the mechanisms underlying this evolutionary success:
Mechanisms of Wolbachia-induced CI:
Wolbachia are widespread in terrestrial arthropod species thanks to powerful strategies of host reproduction manipulation ensuring their matriline transmission. The most common, called Cytoplasmic Incompatibility -CI-, is a conditional sterility syndrome relying on a secreted Toxin-Antitoxin system (CidB and CidA) and occurring when a Wolbachia-infected male inseminates a female which is either non-infected or harbors another incompatible Wolbachia strain. Fertilized eggs resulting from this CI cross usually arrest at very early stages of development, due to paternal chromosomes segregation defects during the first zygotic division. When the female host is infected with a compatible Wolbachia strain, the development is allowed and the Wolbachia are successfully passed through the eggs. By favoring infected over uninfected females, CI enables Wolbachia transmission and spread within arthropod populations. To access the detailed mechanisms of the Toxin-Antitoxin -TA- system on which CI relies, we developed insect cell and yeast models and we are now exploring in detail how DNA replication is poisoned by the CidB toxin (collaborations with the Loppin, Schwob and Weill labs).
Comparative symbiosis studies to comprehend CI.
Is DNA replication always the target in CI? Other symbionts induce CI with putative TA systems such as Rickettsia and Ricketsiella symbionts. We are exploring these unknown mechanisms of CI in tick species (collaboration with the Duron lab).
Wolbachia mutualism in Parasitic Nematodes: what are the cellular and developmental roles of Wolbachia in filarial worms to sustain fertility and survival?
Filarial nematodes are transmitted by blood-feeding arthropods to terrestrial vertebrates. Leading to highly debilitating diseases in humans and even lethal for some animals, all filarial species of biomedical relevance but one live in mutualistic symbiosis with Wolbachia. Depletion of Wolbachia leads to sterility and greatly reduce their lifespan. For a long time, filarial cell biology was limited to immunohistochemistry on cross-sections, poorly informative. We have developed cellular/developmental approaches and RNAseq techniques on dissected tissues to approach the role of Wolbachia in this mutualistic symbiosis, with a focus on the role of Wolbachia in the germline.
Environmental effects on complex parasitic interactions : Characterizing the Blastophage wasp / Wolbachia symbiosis, the wasp / Schistonchus nematode interactions, and the influence of temperature et Ozone pollution.
We have stablished that the fig tree pollinator, Blastophaga psenes, is Wolbachia-infected. This wasp is also the vector of Schistonchus caprifici nematodes. we analyze the interactions between these organisms using wild material (collected from caprifigs in the Montpellier countryside), and establish precisely the life cycle of these nematodes. In collaboration with Finn Kjellberg and Magali Proffit (CEFE), we are investigating the detrimental effects of ozone pollution and temperature increase. Exposed to such conditions, not only the plan-pollinator interaction is lost, but the Blastophage larval/nymphal lethality increases, suggesting possible impacts on the reproduction of surviving adults. Taken together, the fig/blastophage/Wolbachia/Schistonchus is an outstanding model to study and report the highly detrimental effect of Ozone at different scales in Nature, by focusing on the reproduction and development of these interconnected species.
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Financements
ANR WOLF (01/10/2021 – 30/09/2025)
ANR CYTOTIKS (01/10/2025 – 30/09/2029)
Publications
2025
- Host environment shapes filarial parasite fitness and Wolbachia endosymbionts dynamics. Fercoq F, Cormerais C, Remion E, Gal J, Plisson J, Fall A, Alonso J, Lhermitte-Vallarino N, Hübner MP, Kohl L, Landmann F, Martin C. PLoS Pathog. 2025 Jul 11;21(7):e1013301. Pubmed
- Recombination, truncation and horizontal transfer shape the diversity of Wolbachia-induced cytoplasmic incompatibility patterns. Namias A, Martinez J, Boussou I, Terretaz K, Conner W, Justy F, Makoundou P, Perriat-Sanguinet M, Labbé P, Sicard M, Landmann F, Weill M. Mol Biol Evol. 2025 Aug 12:msaf200. Pubmed
2023
- Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication. Terretaz K, Horard B, Weill M, Loppin B, Landmann F. PLoS Pathog. 2023 Mar 16;19(3):e1011211. Pubmed
2022
- Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility. Horard B, Terretaz K, Gosselin-Grenet AS, Sobry H, Sicard M, Landmann F, Loppin B. Curr Biol. 2022 Mar 28;32(6):1319-1331.e5. Pubmed
- A qPCR to quantify Wolbachia from few Onchocerca volvulus microfilariae as a surrogate for adult worm histology in clinical trials of antiwolbachial drugs. Schlabe S, Korir P, Lämmer C, Landmann F, Dubben B, Koschel M, Albers A, Debrah LB, Debrah AY, Hübner MP, Pfarr K, Klarmann-Schulz U, Hoerauf A. Parasitol Res. 2022 Jan 10. Epub ahead of print. Pubmed
2021
- Cytoplasmic Incompatibility Variations in Relation with Wolbachia cid Genes Divergence in Culex pipiens. Sicard M, Namias A, Perriat-Sanguinet M, Carron E, Unal S, Altinli M, Landmann F, Weill M. mBio. 12(1):e02797-20 Pubmed
- Dual RNAseq analyses at soma and germline levels reveal evolutionary innovations in the elephantiasis-agent Brugia malayi, and adaptation of its Wolbachia endosymbionts. Chevignon G, Foray V, Pérez-Jiménez MM, Libro S, Chung M, Foster JM, Landmann F. PLoS Negl Trop Dis. 15(1):e0008935 Pubmed
2019
- IL-4 receptor dependent expansion of lung CD169+ macrophages in microfilaria-driven inflammation. Fercoq F, Remion E, Frohberger SJ, Vallarino-Lhermitte N, Hoerauf A, Le Quesne J, Landmann F, Hübner MP, Carlin LM, Martin C. PLoS Negl Trop Dis ;13(8):e0007691 Pubmed
- Discovery of short-course antiwolbachial quinazolines for elimination of filarial worm infections. Bakowski MA, Shiroodi RK, Liu R, Olejniczak J, Yang B, Gagaring K, Guo H, White PM, Chappell L, Debec A, Landmann F, Dubben B, Lenz F, Struever D, Ehrens A, Frohberger SJ, Sjoberg H, Pionnier N, Murphy E, Archer J, Steven A, Chunda VC, Fombad FF, Chounna PW, Njouendou AJ, Metuge HM, Ndzeshang BL, Gandjui NV, Akumtoh DN, Kwenti TDB, Woods AK, Joseph SB, Hull MV, Xiong W, Kuhen KL, Taylor MJ, Wanji S, Turner JD, Hübner MP, Hoerauf A, Chatterjee AK, Roland J, Tremblay MS, Schultz PG, Sullivan W, Chu XJ, Petrassi HM, McNamara CW. Sci Transl Med ;11(491):eaav3523 Pubmed
- Wolbachia endosymbionts subvert the endoplasmic reticulum to acquire host membranes without triggering ER stress. Fattouh N, Cazevieille C, Landmann F. PLoS Negl Trop Dis. 13(3):e0007218. Pubmed
- The Wolbachia Endosymbionts. Landmann F. Microbiol Spectr. 7(2). Pubmed
2018
- The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity. Manon Bonneau, Frédéric Landmann, Pierrick Labbé, Fabienne Justy, Mylène Weill, Mathieu Sicard. PLoS Pathog; 14(10):e1007364. Pubmed
- Wolbachia Control Stem Cell Behavior and Stimulate Germline Proliferation in Filarial Nematodes. Foray V, Pérez-Jiménez MM, Fattouh N, Landmann F. Dev Cell. 45(2):198-211. Pubmed
2016
- Non-centrosomal epidermal microtubules act in parallel to LET-502/ROCK to promote C. elegans elongation. Quintin S, Wang S, Pontabry J, Bender A, Robin F, Hyenne V, Landmann F, Gally C, Oegema K, Labouesse M. Development. 143:160-73. Pubmed
2014
- Drosophila protamine-like Mst35Ba and Mst35Bb are required for proper sperm nuclear morphology but are dispensable for male fertility. Tirmarche S, Kimura S, Sapey-Triomphe L, Sullivan W, Landmann F, Loppin B. G3 (Bethesda). 4:2241-5. Pubmed
- Co-evolution between an endosymbiont and its nematode host: Wolbachia asymmetric posterior localization and AP polarity establishment. Landmann F, Foster JM, Michalski ML, Slatko BE, Sullivan W. PLoS Negl Trop Dis. 28:e3096. Pubmed
- Absence of Wolbachia endobacteria in the human parasitic nematode Dracunculus medinensis and two related Dracunculus species infecting wildlife. Foster JM, Landmann F, Ford L, Johnston KL, Elsasser SC, Schulte-Hostedde AI, Taylor MJ, Slatko BE. Parasit Vectors. 7:140. Pubmed
2013
- Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Wu B, Novelli J, Jiang D, Dailey HA, Landmann F, Ford L, Taylor MJ, Carlow CK, Kumar S, Foster JM, Slatko BE. Proc Natl Acad Sci U S A. 110(19):7748-53. Pubmed
2012
- Efficient in vitro RNA interference and immunofluorescence-based phenotype analysis in a human parasitic nematode, Brugia malayi. Landmann F, Foster JM, Slatko BE, Sullivan W. Parasit Vectors. 5:16. Pubmed
- A cell-based screen reveals that the albendazole metabolite, albendazole sulfone, targets Wolbachia. Serbus LR, Landmann F, Bray WM, White PM, Ruybal J, Lokey RS, Debec A, Sullivan W. PLoS Pathog. 8(9):e1002922. Pubmed
- A new type F Wolbachia from Splendidofilariinae (Onchocercidae) supports the recent emergence of this supergroup. Lefoulon E, Gavotte L, Junker K, Barbuto M, Uni S, Landmann F, Laaksonen S, Saari S, Nikander S, de Souza Lima S, Casiraghi M, Bain O, Martin C. Int J Parasitol. 42(11):1025-36. Pubmed
- Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Landmann F, Bain O, Martin C, Uni S, Taylor MJ, Sullivan W. Biol Open. 1(6):536-47. Pubmed
2011
- A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Zhang H, Landmann F, Zahreddine H, Rodriguez D, Koch M, Labouesse M. Nature. 471(7336):99-103. Pubmed
- New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza Lima S, Bandi C, Wanji S, Diagne M, Casiraghi M. PLoS One. 6(6):e20843. Pubmed
- Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. Landmann F, Voronin D, Sullivan W, Taylor MJ. PLoS Pathog. 7(11):e1002351. Pubmed
2010
- Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. Landmann F, Foster JM, Slatko B, Sullivan W. PLoS Negl Trop Dis. 4(7):e758. Pubmed
2009
- Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. Landmann F, Orsi GA, Loppin B, Sullivan W. PLoS Pathog. 5(3):e1000343. Pubmed
- Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles. Gally C, Wissler F, Zahreddine H, Quintin S, Landmann F, Labouesse M. Development. 136(18):3109-19. Pubmed
2008
- The genetics and cell biology of Wolbachia-host interactions. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W. Annu Rev Genet. 42:683-707. Pubmed
Mechanisms of symbiosis with Wolbachia
Frédéric Landmann
Group Leader (Research Director CNRS)
Team Members
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HIGHLIGHT August 2025
