Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization

Yan Zhang,Mikhail S Gelfand,Dmitry A Rodionov,Vadim N Gladyshev

doi:10.1186/1471-2164-10-78

Abstract

BackgroundNickel (Ni) and cobalt (Co) are trace elements required for a variety of biological processes. Ni is directly coordinated by proteins, whereas Co is mainly used as a component of vitamin B12. Although a number of Ni and Co-dependent enzymes have been characterized, systematic evolutionary analyses of utilization of these metals are limited.ResultsWe carried out comparative genomic analyses to examine occurrence and evolutionary dynamics of the use of Ni and Co at the level of (i) transport systems, and (ii) metalloproteomes. Our data show that both metals are widely used in bacteria and archaea. Cbi/NikMNQO is the most common prokaryotic Ni/Co transporter, while Ni-dependent urease and Ni-Fe hydrogenase, and B12-dependent methionine synthase (MetH), ribonucleotide reductase and methylmalonyl-CoA mutase are the most widespread metalloproteins for Ni and Co, respectively. Occurrence of other metalloenzymes showed a mosaic distribution and a new B12-dependent protein family was predicted. Deltaproteobacteria and Methanosarcina generally have larger Ni- and Co-dependent proteomes. On the other hand, utilization of these two metals is limited in eukaryotes, and very few of these organisms utilize both of them. The Ni-utilizing eukaryotes are mostly fungi (except saccharomycotina) and plants, whereas most B12-utilizing organisms are animals. The NiCoT transporter family is the most widespread eukaryotic Ni transporter, and eukaryotic urease and MetH are the most common Ni- and B12-dependent enzymes, respectively. Finally, investigation of environmental and other conditions and identity of organisms that show dependence on Ni or Co revealed that host-associated organisms (particularly obligate intracellular parasites and endosymbionts) have a tendency for loss of Ni/Co utilization.ConclusionOur data provide information on the evolutionary dynamics of Ni and Co utilization and highlight widespread use of these metals in the three domains of life, yet only a limited number of user proteins.

Highlights

Nickel (Ni) and cobalt (Co) are trace elements required for a variety of biological processes
Considering that members of most non-corrin Cobinding proteins may bind other metal cofactors instead of Co, we only focused on the utilization of the corrin form of Co, whose utilization could be predicted on the basis of B12 biosynthesis pathway and B12-dependent protein families
Occurrence of nickel and cobalt utilization in prokaryotes and eukaryotes Analysis of prokaryotic genomes revealed a wide distribution of genes encoding Ni and Co transporters as well as Ni- and Co-dependent proteins [see Additional files 1 and 2]

Summary

Introduction

Nickel (Ni) and cobalt (Co) are trace elements required for a variety of biological processes. A number of Ni and Co-dependent enzymes have been characterized, systematic evolutionary analyses of utilization of these metals are limited. Several trace elements are utilized, including certain metals and metalloids. Because these elements play important roles in cellular metabolism, efficient mechanisms of uptake, storage and utilization are required for many of them. Nickel (Ni) and cobalt (Co) are utilized at low levels but play important roles in several biological systems. Additional candidate Ni-containing proteins or compounds have been described in different organisms including humans [9]

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