TY - JOUR
T1 - From conservation to structure, studies of magnetosome associated cation diffusion facilitators (CDF) proteins in Proteobacteria
AU - Keren-Khadmy, Noa
AU - Zeytuni, Natalie
AU - Kutnowski, Nitzan
AU - Perriere, Guy
AU - Monteil, Caroline
AU - Zarivach, Raz
N1 - Funding Information:
Funding:Theauthorsofthisworkaresupported bytheIsraelMinistryofScience,Technology,and Space(R.Z.),theIsraelScienceFoundation(grant No.167/16;R.Z.)andtheEuropeanMolecular BiologyOrganizationandCMSTCOSTAction CM1306(R.Z.).Thefundershadnoroleinstudy design,datacollectionandanalysis,decisionto publish,orpreparationofthemanuscript.
Funding Information:
? 2020 Keren-Khadmy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The authors of this work are supported by the Israel Ministry of Science, Technology, and Space (R.Z.), the Israel Science Foundation (grant No. 167/16; R.Z.) and the European Molecular Biology Organization and CMST COST Action CM1306 (R.Z.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank ESRF (Grenoble, France) for providing synchrotron radiation facilities beamline ID23-2 and ID14-4 and for assistance during data collection, and Dr. Petra Pernot for assistance in using beamline BM29-bioSAXS. We thank the 1st CCP4/BGU Structural Solution Workshop and especially to Dr. Kay Diederichs and Dr. Michael Yosephov who assisted in data processing and structure determination of MamM-CTD. Without their professional help, we would not have been able to determine this structure. We thank Dr. Anat Shahar from the Macromolecular Crystallography Research Center (Ben-Gurion University of the Negev, Israel). We thank Dr. Hila Nudelman and Dr. Shiran Barber-Zucker for a fruitful discussion and good scientific advice. The authors are grateful to the INRAE Migale bioinformatics platform (https://migale.inra.fr) for providing computational resources.
Publisher Copyright:
© 2020 Public Library of Science. All rights reserved.
PY - 2020/4/1
Y1 - 2020/4/1
N2 - Magnetotactic bacteria (MTB) are prokaryotes that sense the geomagnetic field lines to geolocate and navigate in aquatic sediments. They are polyphyletically distributed in several bacterial divisions but are mainly represented in the Proteobacteria. In this phylum, magnetotactic Deltaproteobacteria represent the most ancestral class of MTB. Like all MTB, they synthesize membrane-enclosed magnetic nanoparticles, called magnetosomes, for magnetic sensing. Magnetosome biogenesis is a complex process involving a specific set of genes that are conserved across MTB. Two of the most conserved genes are mamB and mamM, that encode for the magnetosome-associated proteins and are homologous to the cation diffusion facilitator (CDF) protein family. In magnetotactic Alphaproteobacteria MTB species, MamB and MamM proteins have been well characterized and play a central role in iron-transport required for biomineralization. However, their structural conservation and their role in more ancestral groups of MTB like the Deltaproteobacteria have not been established. Here we studied magnetite cluster MamB and MamM cytosolic C-terminal domain (CTD) structures from a phylogenetically distant magnetotactic Deltaproteobacteria species represented by BW-1 strain, which has the unique ability to biomineralize magnetite and greigite. We characterized them in solution, analyzed their crystal structures and compared them to those characterized in Alphaproteobacteria MTB species. We showed that despite the high phylogenetic distance, MamBBW-1 and MamMBW-1 CTDs share high structural similarity with known CDF-CTDs and will probably share a common function with the Alphaproteobacteria MamB and MamM.
AB - Magnetotactic bacteria (MTB) are prokaryotes that sense the geomagnetic field lines to geolocate and navigate in aquatic sediments. They are polyphyletically distributed in several bacterial divisions but are mainly represented in the Proteobacteria. In this phylum, magnetotactic Deltaproteobacteria represent the most ancestral class of MTB. Like all MTB, they synthesize membrane-enclosed magnetic nanoparticles, called magnetosomes, for magnetic sensing. Magnetosome biogenesis is a complex process involving a specific set of genes that are conserved across MTB. Two of the most conserved genes are mamB and mamM, that encode for the magnetosome-associated proteins and are homologous to the cation diffusion facilitator (CDF) protein family. In magnetotactic Alphaproteobacteria MTB species, MamB and MamM proteins have been well characterized and play a central role in iron-transport required for biomineralization. However, their structural conservation and their role in more ancestral groups of MTB like the Deltaproteobacteria have not been established. Here we studied magnetite cluster MamB and MamM cytosolic C-terminal domain (CTD) structures from a phylogenetically distant magnetotactic Deltaproteobacteria species represented by BW-1 strain, which has the unique ability to biomineralize magnetite and greigite. We characterized them in solution, analyzed their crystal structures and compared them to those characterized in Alphaproteobacteria MTB species. We showed that despite the high phylogenetic distance, MamBBW-1 and MamMBW-1 CTDs share high structural similarity with known CDF-CTDs and will probably share a common function with the Alphaproteobacteria MamB and MamM.
UR - http://www.scopus.com/inward/record.url?scp=85083568623&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0231839
DO - 10.1371/journal.pone.0231839
M3 - Article
C2 - 32310978
AN - SCOPUS:85083568623
VL - 15
JO - PLoS ONE
JF - PLoS ONE
SN - 1932-6203
IS - 4
M1 - e0231839
ER -