Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans

Annelie Persson*, Einav Gross, Patrick Laurent, Karl Emanuel Busch, Hugo Bretes, Mario De Bono

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

109 Scopus citations

Abstract

Behaviours evolve by iterations of natural selection, but we have few insights into the molecular and neural mechanisms involved. Here we show that some Caenorhabditis elegans wild strains switch between two foraging behaviours in response to subtle changes in ambient oxygen. This finely tuned switch is conferred by a naturally variable hexacoordinated globin, GLB-5. GLB-5 acts with the atypical soluble guanylate cyclases, which are a different type of oxygen binding protein, to tune the dynamic range of oxygen-sensing neurons close to atmospheric (21%) concentrations. Calcium imaging indicates that one group of these neurons is activated when oxygen rises towards 21%, and is inhibited as oxygen drops below 21%. The soluble guanylate cyclase GCY-35 is required for high oxygen to activate the neurons; GLB-5 provides inhibitory input when oxygen decreases below 21%. Together, these oxygen binding proteins tune neuronal and behavioural responses to a narrow oxygen concentration range close to atmospheric levels. The effect of the glb-5 gene on oxygen sensing and foraging is modified by the naturally variable neuropeptide receptor npr-1 (refs 4, 5), providing insights into how polygenic variation reshapes neural circuit function.

Original languageAmerican English
Pages (from-to)1030-1033
Number of pages4
JournalNature
Volume458
Issue number7241
DOIs
StatePublished - 23 Apr 2009
Externally publishedYes

Bibliographical note

Funding Information:
Acknowledgements We thank the Caenorhabditis Genetics Center, A. Chisholm, M.-A. Felix and E. Dolgin for C. elegans strains, A. Couto, B. Olofsson, I. Rabinovitch and K. Weber for comments on the manuscript, and I. Johnston and C. Tan for microfluidic devices. This work was supported by the Medical Research Council, a Human Frontier Science Program (HFSP) long-term fellowship (E.G.) and program grant (M.d.B.), the EU Marie Curie Actions (K.E.B.), the European Molecular Biology Organization (K.E.B. and P.L.) and the Fondation Wiener–Anspach (P.L.).

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