Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells.
Nature Publishing Group
This is the final version of the article. Available from the publisher via the DOI in this record.
Even distribution of peroxisomes (POs) and lipid droplets (LDs) is critical to their role in lipid and reactive oxygen species homeostasis. How even distribution is achieved remains elusive, but diffusive motion and directed motility may play a role. Here we show that in the fungus Ustilago maydis ∼95% of POs and LDs undergo diffusive motions. These movements require ATP and involve bidirectional early endosome motility, indicating that microtubule-associated membrane trafficking enhances diffusion of organelles. When early endosome transport is abolished, POs and LDs drift slowly towards the growing cell end. This pole-ward drift is facilitated by anterograde delivery of secretory cargo to the cell tip by myosin-5. Modelling reveals that microtubule-based directed transport and active diffusion support distribution, mobility and mixing of POs. In mammalian COS-7 cells, microtubules and F-actin also counteract each other to distribute POs. This highlights the importance of opposing cytoskeletal forces in organelle positioning in eukaryotes.
We thank Dr G. Dagdas, Dr S. Kilaru, Mr M. Schlick and Mrs T. Schrader for technical support. We thank Professor N.J. Talbot for helpful comments on the manuscript. This work was supported by the Biotechnology & Biological Sciences Research Council (BB/J009903/1 to G.S.). S.C.G. was supported by a fellowship from the Portuguese Foundation for Science and Technology (FCT) (SFRH/BD/73532/2010). J.M. is supported by a Wellcome Trust Institutional Strategic Support Award (WT097835MF).
Nature Communications, 2016, Vol. 7, Article number 11814
Place of publication