TY - JOUR
T1 - A role for copper in protozoan grazing – two billion years selecting for bacterial copper resistance
AU - Hao, Xiuli
AU - Lüthje, Freja
AU - Rønn, Regin
AU - German, Nadezhda A.
AU - Li, Xuanji
AU - Huang, Fuyi
AU - Kisaka, Javan
AU - Huffman, David
AU - Alwathnani, Hend A.
AU - Zhu, Yong Guan
AU - Rensing, Christopher
N1 - Funding Information:
This work is supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020402 and XDB15020302), the International Postdoctoral Exchange Fellowship Program (No. 20150079) awarded by the Office of China Postdoctoral Council, and in part supported by a grant from the Support for Faculty Scholars Award at Western Michigan University (DLH) (Project S2015-017). DLH would like to thank the Danish-American Fulbright Commission for a Fulbright Senior Scholar grant. We gratefully thank Dr. Hu-Chun Tao (Peking University Shenzhen Graduate School, China) for providing the copper-sensor strain, Nanna Svenningsen for the gift of ROS biosensor strain P. putida (pKatA), and Nynne Meyn Christensen (Center for Advanced Bioimaging, CAB) and Birger Brodin Larsen (Department of Pharmacy, University of Copenhagen) for help with confocal laser microscopy.
Publisher Copyright:
© 2016 John Wiley & Sons Ltd
PY - 2016/11/1
Y1 - 2016/11/1
N2 - The Great Oxidation Event resulted in integration of soft metals in a wide range of biochemical processes including, in our opinion, killing of bacteria by protozoa. Compared to pressure from anthropologic copper contamination, little is known on impacts of protozoan predation on maintenance of copper resistance determinants in bacteria. To evaluate the role of copper and other soft metals in predatory mechanisms of protozoa, we examined survival of bacteria mutated in different transition metal efflux or uptake systems in the social amoeba Dictyostelium discoideum. Our data demonstrated a strong correlation between the presence of copper/zinc efflux as well as iron/manganese uptake, and bacterial survival in amoebae. The growth of protozoa, in turn, was dependent on bacterial copper sensitivity. The phagocytosis of bacteria induced upregulation of Dictyostelium genes encoding the copper uptake transporter p80 and a triad of Cu(I)-translocating PIB-type ATPases. Accumulated Cu(I) in Dictyostelium was monitored using a copper biosensor bacterial strain. Altogether, our data demonstrate that Cu(I) is ultimately involved in protozoan predation of bacteria, supporting our hypothesis that protozoan grazing selected for the presence of copper resistance determinants for about two billion years.
AB - The Great Oxidation Event resulted in integration of soft metals in a wide range of biochemical processes including, in our opinion, killing of bacteria by protozoa. Compared to pressure from anthropologic copper contamination, little is known on impacts of protozoan predation on maintenance of copper resistance determinants in bacteria. To evaluate the role of copper and other soft metals in predatory mechanisms of protozoa, we examined survival of bacteria mutated in different transition metal efflux or uptake systems in the social amoeba Dictyostelium discoideum. Our data demonstrated a strong correlation between the presence of copper/zinc efflux as well as iron/manganese uptake, and bacterial survival in amoebae. The growth of protozoa, in turn, was dependent on bacterial copper sensitivity. The phagocytosis of bacteria induced upregulation of Dictyostelium genes encoding the copper uptake transporter p80 and a triad of Cu(I)-translocating PIB-type ATPases. Accumulated Cu(I) in Dictyostelium was monitored using a copper biosensor bacterial strain. Altogether, our data demonstrate that Cu(I) is ultimately involved in protozoan predation of bacteria, supporting our hypothesis that protozoan grazing selected for the presence of copper resistance determinants for about two billion years.
UR - http://www.scopus.com/inward/record.url?scp=84984706615&partnerID=8YFLogxK
U2 - 10.1111/mmi.13483
DO - 10.1111/mmi.13483
M3 - Article
C2 - 27528008
AN - SCOPUS:84984706615
SN - 0950-382X
VL - 102
SP - 628
EP - 641
JO - Molecular Microbiology
JF - Molecular Microbiology
IS - 4
ER -