A comprehensive phylogenetic analysis of copper transporting P_1B ATPases from bacteria of the Rhizobiales order uncovers multiplicity, diversity and novel taxonomic subtypes

Abstract

The ubiquitous cytoplasmic membrane copper transporting P1B‐1 and P1B‐3‐type ATPases pump out Cu+ and Cu2+, respectively, to prevent cytoplasmic accumulation and avoid toxicity. The presence of five copies of Cu‐ATPases in the symbiotic nitrogen‐fixing bacteria Sinorhizobium meliloti is remarkable; it is the largest number of Cu+‐transporters in a bacterial genome reported to date. Since the prevalence of multiple Cu‐ATPases in members of the Rhizobiales order is unknown, we performed an in silico analysis to understand the occurrence, diversity and evolution of Cu+‐ATPases in members of the Rhizobiales order. Multiple copies of Cu‐ATPase coding genes (2–8) were detected in 45 of the 53 analyzed genomes. The diversity inferred from a maximum‐likelihood (ML) phylogenetic analysis classified Cu‐ATPases into four monophyletic groups. Each group contained additional subtypes, based on the presence of conserved motifs. This novel phylogeny redefines the current classification, where they are divided into two subtypes (P1B‐1 and P1B‐3). Horizontal gene transfer (HGT) as well as the evolutionary dynamic of plasmid‐borne genes may have played an important role in the functional diversification of Cu‐ATPases. Homologous cytoplasmic and periplasmic Cu+‐chaperones, CopZ, and CusF, that integrate a CopZ‐CopA‐CusF tripartite efflux system in gamma‐proteobacteria and archeae, were found in 19 of the 53 surveyed genomes of the Rhizobiales. This result strongly suggests a high divergence of CopZ and CusF homologs, or the existence of unexplored proteins involved in cellular copper transport.

Identification and Characterization of a Novel pic Gene Cluster Responsible for Picolinic Acid Degradation in Alcaligenes faecalis JQ135

“…strain JS1663 (40,41), human pathogens (e.g., Bordetella pertussis Tohama I and Bordetella bronchiseptica RB50) (42), and nematicidal bacteria (e.g., A. faecalis ZD02) (43), whereas other strains represent typical soil bacteria (e.g., Pseudomonas), plant rhizosphere-associated bacteria (e.g., Bradyrhizobium), arctic bacteria (Octadecabacter arcticus 238) (44), and Antarctic bacteria (Hoeflea sp. strain IMCC20628) (45).) Three of predicted degraders listed in Table S1 (A. faecalis ATCC 8750, Cupriavidus pinatubonensis JMP134 [46], and Pusillimonas sp.…”

The Role of the CopA Copper Efflux System in Acinetobacter baumannii Virulence

“…Further bioinformatic analyses revealed that CueA of A. baumannii belongs to a distinct group of P 1B-1 ATPases, which we denoted the “histidine-rich” subgroup. P 1B-1 ATPases with an elevated number of histidine residues have been previously described in the analysis of P-type ATPases from the Rhizobiales order, which includes nitrogen-fixing plant symbionts, such as the Sinorhizobium species, and the human pathogens of the Bartonella species [34]. Although none of the histidine-rich P 1B-1 ATPases from Sinorhizobium species have been functionally characterised, the roles of LpCopA and SilP in metal resistance illustrate that the histidine-rich P 1B-1 ATPases can fulfil important roles.…”

Copper homeostasis networks in the bacterium Pseudomonas aeruginosa

“…The role of Cu ϩ chaperone proteins mobilizing the metal within compartments has been characterized (24,25). In some organisms, a periplasmic chaperone (CusF) associated with the RND-type efflux system is also present (26,27). On the other hand, organisms apparently lacking cytoplasmic or periplasmic chaperones have been identified (27).…”