IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38706-z.html
   My bibliography  Save this article

Plasmodium sporozoite search strategy to locate hotspots of blood vessel invasion

Author

Listed:
  • Pauline Formaglio

    (Université Paris Cité, Malaria Infection and Immunity Unit)

  • Marina E. Wosniack

    (Max Planck Institute for Brain Research)

  • Raphael M. Tromer

    (Universidade Federal do Rio Grande do Norte)

  • Jaderson G. Polli

    (Universidade Federal do Paraná)

  • Yuri B. Matos

    (Universidade Federal do Paraná)

  • Hang Zhong

    (Université Paris Cité, Malaria Infection and Immunity Unit)

  • Ernesto P. Raposo

    (Universidade Federal de Pernambuco)

  • Marcos G. E. Luz

    (Universidade Federal do Paraná)

  • Rogerio Amino

    (Université Paris Cité, Malaria Infection and Immunity Unit)

Abstract

Plasmodium sporozoites actively migrate in the dermis and enter blood vessels to infect the liver. Despite their importance for malaria infection, little is known about these cutaneous processes. We combine intravital imaging in a rodent malaria model and statistical methods to unveil the parasite strategy to reach the bloodstream. We determine that sporozoites display a high-motility mode with a superdiffusive Lévy-like pattern known to optimize the location of scarce targets. When encountering blood vessels, sporozoites frequently switch to a subdiffusive low-motility behavior associated with probing for intravasation hotspots, marked by the presence of pericytes. Hence, sporozoites present anomalous diffusive motility, alternating between superdiffusive tissue exploration and subdiffusive local vessel exploitation, thus optimizing the sequential tasks of seeking blood vessels and pericyte-associated sites of privileged intravasation.

Suggested Citation

  • Pauline Formaglio & Marina E. Wosniack & Raphael M. Tromer & Jaderson G. Polli & Yuri B. Matos & Hang Zhong & Ernesto P. Raposo & Marcos G. E. Luz & Rogerio Amino, 2023. "Plasmodium sporozoite search strategy to locate hotspots of blood vessel invasion," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38706-z
    DOI: 10.1038/s41467-023-38706-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38706-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38706-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Marina E Wosniack & Marcos C Santos & Ernesto P Raposo & Gandhi M Viswanathan & Marcos G E da Luz, 2017. "The evolutionary origins of Lévy walk foraging," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-31, October.
    2. Minho S. Song & Hyungseok C. Moon & Jae-Hyung Jeon & Hye Yoon Park, 2018. "Neuronal messenger ribonucleoprotein transport follows an aging Lévy walk," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    3. G. M. Viswanathan & Sergey V. Buldyrev & Shlomo Havlin & M. G. E. da Luz & E. P. Raposo & H. Eugene Stanley, 1999. "Optimizing the success of random searches," Nature, Nature, vol. 401(6756), pages 911-914, October.
    4. David W. Sims & Emily J. Southall & Nicolas E. Humphries & Graeme C. Hays & Corey J. A. Bradshaw & Jonathan W. Pitchford & Alex James & Mohammed Z. Ahmed & Andrew S. Brierley & Mark A. Hindell & David, 2008. "Scaling laws of marine predator search behaviour," Nature, Nature, vol. 451(7182), pages 1098-1102, February.
    5. Gillespie, Colin S., 2015. "Fitting Heavy Tailed Distributions: The poweRlaw Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 64(i02).
    6. Henrik Seckler & Ralf Metzler, 2022. "Bayesian deep learning for error estimation in the analysis of anomalous diffusion," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Toman, Kellan & Voulgarakis, Nikolaos K., 2022. "Stochastic pursuit-evasion curves for foraging dynamics," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 597(C).
    2. Ferreira, A.S. & Raposo, E.P. & Viswanathan, G.M. & da Luz, M.G.E., 2012. "The influence of the environment on Lévy random search efficiency: Fractality and memory effects," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(11), pages 3234-3246.
    3. Cody T Ross & Bruce Winterhalder, 2018. "Evidence for encounter-conditional, area-restricted search in a preliminary study of Colombian blowgun hunters," PLOS ONE, Public Library of Science, vol. 13(12), pages 1-13, December.
    4. LaScala-Gruenewald, Diana E. & Mehta, Rohan S. & Liu, Yu & Denny, Mark W., 2019. "Sensory perception plays a larger role in foraging efficiency than heavy-tailed movement strategies," Ecological Modelling, Elsevier, vol. 404(C), pages 69-82.
    5. Danish A. Ahmed & Sergei V. Petrovskii & Paulo F. C. Tilles, 2018. "The “Lévy or Diffusion” Controversy: How Important Is the Movement Pattern in the Context of Trapping?," Mathematics, MDPI, vol. 6(5), pages 1-27, May.
    6. Nauta, Johannes & Simoens, Pieter & Khaluf, Yara, 2022. "Group size and resource fractality drive multimodal search strategies: A quantitative analysis on group foraging," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 590(C).
    7. E P Raposo & F Bartumeus & M G E da Luz & P J Ribeiro-Neto & T A Souza & G M Viswanathan, 2011. "How Landscape Heterogeneity Frames Optimal Diffusivity in Searching Processes," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-8, November.
    8. Sepideh Bazazi & Frederic Bartumeus & Joseph J Hale & Iain D Couzin, 2012. "Intermittent Motion in Desert Locusts: Behavioural Complexity in Simple Environments," PLOS Computational Biology, Public Library of Science, vol. 8(5), pages 1-10, May.
    9. Masato S Abe & Masakazu Shimada, 2015. "Lévy Walks Suboptimal under Predation Risk," PLOS Computational Biology, Public Library of Science, vol. 11(11), pages 1-16, November.
    10. Danish A Ahmed & Ali R Ansari & Mudassar Imran & Kamal Dingle & Michael B Bonsall, 2021. "Mechanistic modelling of COVID-19 and the impact of lockdowns on a short-time scale," PLOS ONE, Public Library of Science, vol. 16(10), pages 1-20, October.
    11. Boschetti, Fabio & Vanderklift, Mathew A., 2015. "How the movement characteristics of large marine predators influence estimates of their abundance," Ecological Modelling, Elsevier, vol. 313(C), pages 223-236.
    12. Toby A. Patterson & Alison Parton & Roland Langrock & Paul G. Blackwell & Len Thomas & Ruth King, 2017. "Statistical modelling of individual animal movement: an overview of key methods and a discussion of practical challenges," AStA Advances in Statistical Analysis, Springer;German Statistical Society, vol. 101(4), pages 399-438, October.
    13. Shinohara, Shuji & Okamoto, Hiroshi & Manome, Nobuhito & Gunji, Pegio-Yukio & Nakajima, Yoshihiro & Moriyama, Toru & Chung, Ung-il, 2022. "Simulation of foraging behavior using a decision-making agent with Bayesian and inverse Bayesian inference: Temporal correlations and power laws in displacement patterns," Chaos, Solitons & Fractals, Elsevier, vol. 157(C).
    14. Filippo Radicchi & Andrea Baronchelli & Luís A N Amaral, 2012. "Rationality, Irrationality and Escalating Behavior in Lowest Unique Bid Auctions," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-8, January.
    15. Goldrosen, Nicholas, 2024. "Is corrections officers' use of illegal force networked? Network structure, brokerage, and key players in the New York City Department of Correction," Journal of Criminal Justice, Elsevier, vol. 92(C).
    16. Priscila C A da Silva & Tiago V Rosembach & Anésia A Santos & Márcio S Rocha & Marcelo L Martins, 2014. "Normal and Tumoral Melanocytes Exhibit q-Gaussian Random Search Patterns," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-13, September.
    17. Lyócsa, Štefan & Výrost, Tomáš, 2018. "Scale-free distribution of firm-size distribution in emerging economies," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 508(C), pages 501-505.
    18. Andy Reynolds & Eliane Ceccon & Cristina Baldauf & Tassia Karina Medeiros & Octavio Miramontes, 2018. "Lévy foraging patterns of rural humans," PLOS ONE, Public Library of Science, vol. 13(6), pages 1-16, June.
    19. Čukić, Milena & Galovic, Slobodanka, 2023. "Mathematical modeling of anomalous diffusive behavior in transdermal drug-delivery including time-delayed flux concept," Chaos, Solitons & Fractals, Elsevier, vol. 172(C).
    20. Musa, Hussam & Krištofík, Peter & Medzihorský, Juraj & Klieštik, Tomáš, 2024. "The development of firm size distribution – Evidence from four Central European countries," International Review of Economics & Finance, Elsevier, vol. 91(C), pages 98-110.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38706-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.