The Crystal Structure of the Ca2+-ATPase 1 from Listeria monocytogenes reveals a Pump Primed for Dephosphorylation

Sara Basse Hansen; Mateusz Dyla; Caroline Neumann; Esben Meldgaard Hoegh Quistgaard; Jacob Lauwring Andersen; Magnus Kjaergaard; Poul Nissen

doi:10.1016/j.jmb.2021.167015

The Crystal Structure of the Ca²⁺-ATPase 1 from Listeria monocytogenes reveals a Pump Primed for Dephosphorylation

Sara Basse Hansen, Mateusz Dyla, Caroline Neumann, Esben Meldgaard Hoegh Quistgaard, Jacob Lauwring Andersen, Magnus Kjaergaard, Poul Nissen^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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Abstract

Many bacteria export intracellular calcium using active transporters homologous to the sarco/endoplasmic reticulum Ca²⁺-ATPase (SERCA). Here we present three crystal structures of Ca²⁺-ATPase 1 from Listeria monocytogenes (LMCA1). Structures with BeF₃^- mimicking a phosphoenzyme state reveal a closed state, which is intermediate between the outward-open E2P and the proton-occluded E2-P* conformations known for SERCA. It suggests that LMCA1 in the E2P state is pre-organized for dephosphorylation upon Ca²⁺ release, consistent with the rapid dephosphorylation observed in single-molecule studies. An arginine side-chain occupies the position equivalent to calcium binding site I in SERCA, leaving a single Ca²⁺ binding site in LMCA1, corresponding to SERCA site II. Observing no putative transport pathways dedicated to protons, we infer a direct proton counter transport through the Ca²⁺ exchange pathways. The LMCA1 structures provide insight into the evolutionary divergence and conserved features of this important class of ion transporters.

Original language	English
Article number	167015
Journal	Journal of Molecular Biology
Volume	433
Issue	16
ISSN	0022-2836
DOIs	https://doi.org/10.1016/j.jmb.2021.167015
Publication status	Published - Aug 2021

Keywords

Ca-ATPase LMCA1
calcium
Listeria
membrane protein crystallography
P-type ATPase

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Cite this

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title = "The Crystal Structure of the Ca2+-ATPase 1 from Listeria monocytogenes reveals a Pump Primed for Dephosphorylation",

abstract = "Many bacteria export intracellular calcium using active transporters homologous to the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA). Here we present three crystal structures of Ca2+-ATPase 1 from Listeria monocytogenes (LMCA1). Structures with BeF3- mimicking a phosphoenzyme state reveal a closed state, which is intermediate between the outward-open E2P and the proton-occluded E2-P* conformations known for SERCA. It suggests that LMCA1 in the E2P state is pre-organized for dephosphorylation upon Ca2+ release, consistent with the rapid dephosphorylation observed in single-molecule studies. An arginine side-chain occupies the position equivalent to calcium binding site I in SERCA, leaving a single Ca2+ binding site in LMCA1, corresponding to SERCA site II. Observing no putative transport pathways dedicated to protons, we infer a direct proton counter transport through the Ca2+ exchange pathways. The LMCA1 structures provide insight into the evolutionary divergence and conserved features of this important class of ion transporters.",

keywords = "Ca-ATPase LMCA1, calcium, Listeria, membrane protein crystallography, P-type ATPase",

author = "Hansen, {Sara Basse} and Mateusz Dyla and Caroline Neumann and Quistgaard, {Esben Meldgaard Hoegh} and Andersen, {Jacob Lauwring} and Magnus Kjaergaard and Poul Nissen",

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The Crystal Structure of the Ca²⁺-ATPase 1 from Listeria monocytogenes reveals a Pump Primed for Dephosphorylation. / Hansen, Sara Basse; Dyla, Mateusz; Neumann, Caroline et al.
In: Journal of Molecular Biology, Vol. 433, No. 16, 167015, 08.2021.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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T1 - The Crystal Structure of the Ca2+-ATPase 1 from Listeria monocytogenes reveals a Pump Primed for Dephosphorylation

AU - Hansen, Sara Basse

AU - Dyla, Mateusz

AU - Neumann, Caroline

AU - Quistgaard, Esben Meldgaard Hoegh

AU - Andersen, Jacob Lauwring

AU - Kjaergaard, Magnus

AU - Nissen, Poul

PY - 2021/8

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N2 - Many bacteria export intracellular calcium using active transporters homologous to the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA). Here we present three crystal structures of Ca2+-ATPase 1 from Listeria monocytogenes (LMCA1). Structures with BeF3- mimicking a phosphoenzyme state reveal a closed state, which is intermediate between the outward-open E2P and the proton-occluded E2-P* conformations known for SERCA. It suggests that LMCA1 in the E2P state is pre-organized for dephosphorylation upon Ca2+ release, consistent with the rapid dephosphorylation observed in single-molecule studies. An arginine side-chain occupies the position equivalent to calcium binding site I in SERCA, leaving a single Ca2+ binding site in LMCA1, corresponding to SERCA site II. Observing no putative transport pathways dedicated to protons, we infer a direct proton counter transport through the Ca2+ exchange pathways. The LMCA1 structures provide insight into the evolutionary divergence and conserved features of this important class of ion transporters.

AB - Many bacteria export intracellular calcium using active transporters homologous to the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA). Here we present three crystal structures of Ca2+-ATPase 1 from Listeria monocytogenes (LMCA1). Structures with BeF3- mimicking a phosphoenzyme state reveal a closed state, which is intermediate between the outward-open E2P and the proton-occluded E2-P* conformations known for SERCA. It suggests that LMCA1 in the E2P state is pre-organized for dephosphorylation upon Ca2+ release, consistent with the rapid dephosphorylation observed in single-molecule studies. An arginine side-chain occupies the position equivalent to calcium binding site I in SERCA, leaving a single Ca2+ binding site in LMCA1, corresponding to SERCA site II. Observing no putative transport pathways dedicated to protons, we infer a direct proton counter transport through the Ca2+ exchange pathways. The LMCA1 structures provide insight into the evolutionary divergence and conserved features of this important class of ion transporters.

KW - Ca-ATPase LMCA1

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KW - membrane protein crystallography

KW - P-type ATPase

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