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Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization.

Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN - BMC Genomics (2009)

Bottom Line: 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.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.Our 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Redox Biology Center, University of Nebraska, Lincoln, NE 68588-0664, USA. yzhang@genomics.unl.edu

ABSTRACT

Background: Nickel (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.

Results: We 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.

Conclusion: Our 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.

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Ni-dependent metalloproteomes in bacteria. For each phylum, all organisms containing Ni-dependent proteins are indicated. Numbers following the name of each phylum represent the number of organisms containing a Ni-binding protein and that of total sequenced organisms, respectively. The largest Ni-dependent metalloproteome was observed in a deltaproteobacterium MLMS-1 (16 Ni-binding proteins).
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Figure 5: Ni-dependent metalloproteomes in bacteria. For each phylum, all organisms containing Ni-dependent proteins are indicated. Numbers following the name of each phylum represent the number of organisms containing a Ni-binding protein and that of total sequenced organisms, respectively. The largest Ni-dependent metalloproteome was observed in a deltaproteobacterium MLMS-1 (16 Ni-binding proteins).

Mentions: Further analyses of the Ni- or Co-dependent metalloproteomes (i.e., sets of Ni- and Co(B12)-dependent enzymes) in different phyla provided us with an opportunity to explore the evolution of these metalloproteomes (Fig. 5, 6, 7). Normalized occurrence of these metalloproteins is shown [see Additional files 22 and 23]. There is no correlation between the number of Ni- or Co-dependent enzymes and the genome/proteome size (data not shown). In most bacteria, the size of the Ni-dependent metalloproteome was 1–4 (Fig. 5). Most of these proteins were ureases or Ni-Fe hydrogenases. However, half of sequenced Deltaproteobacteria appeared to have a larger Ni-dependent metalloproteome (≥ 5), including deltaproteobacterium MLMS-1, which possessed the largest Ni-dependent metalloproteome (16 Ni-binding proteins, half of which were Ni-Fe hydrogenases). Similarly, compared to most Co-utilizing species which had 1–4 Co-dependent metalloenzymes, the majority of organisms in some phyla, such as the Chloroflexi (including two Dehalococcoides species which have the largest number of B12-binding proteins in prokaryotes), Spirochaetales, Actinobacteria and Deltaproteobacteria, had larger Co-dependent metalloproteomes (≥ 5, Fig. 6). Therefore, the Deltaproteobacteria appear to be the only bacterial phylum which favors the use of both metals. In archaea, large Ni- or Co-dependent metalloproteomes were observed in methanogens (Fig. 7). Three Methanosarcina species in the Methanosarcinales phylum had the largest metalloproteomes for both Ni and Co.


Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization.

Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN - BMC Genomics (2009)

Ni-dependent metalloproteomes in bacteria. For each phylum, all organisms containing Ni-dependent proteins are indicated. Numbers following the name of each phylum represent the number of organisms containing a Ni-binding protein and that of total sequenced organisms, respectively. The largest Ni-dependent metalloproteome was observed in a deltaproteobacterium MLMS-1 (16 Ni-binding proteins).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667541&req=5

Figure 5: Ni-dependent metalloproteomes in bacteria. For each phylum, all organisms containing Ni-dependent proteins are indicated. Numbers following the name of each phylum represent the number of organisms containing a Ni-binding protein and that of total sequenced organisms, respectively. The largest Ni-dependent metalloproteome was observed in a deltaproteobacterium MLMS-1 (16 Ni-binding proteins).
Mentions: Further analyses of the Ni- or Co-dependent metalloproteomes (i.e., sets of Ni- and Co(B12)-dependent enzymes) in different phyla provided us with an opportunity to explore the evolution of these metalloproteomes (Fig. 5, 6, 7). Normalized occurrence of these metalloproteins is shown [see Additional files 22 and 23]. There is no correlation between the number of Ni- or Co-dependent enzymes and the genome/proteome size (data not shown). In most bacteria, the size of the Ni-dependent metalloproteome was 1–4 (Fig. 5). Most of these proteins were ureases or Ni-Fe hydrogenases. However, half of sequenced Deltaproteobacteria appeared to have a larger Ni-dependent metalloproteome (≥ 5), including deltaproteobacterium MLMS-1, which possessed the largest Ni-dependent metalloproteome (16 Ni-binding proteins, half of which were Ni-Fe hydrogenases). Similarly, compared to most Co-utilizing species which had 1–4 Co-dependent metalloenzymes, the majority of organisms in some phyla, such as the Chloroflexi (including two Dehalococcoides species which have the largest number of B12-binding proteins in prokaryotes), Spirochaetales, Actinobacteria and Deltaproteobacteria, had larger Co-dependent metalloproteomes (≥ 5, Fig. 6). Therefore, the Deltaproteobacteria appear to be the only bacterial phylum which favors the use of both metals. In archaea, large Ni- or Co-dependent metalloproteomes were observed in methanogens (Fig. 7). Three Methanosarcina species in the Methanosarcinales phylum had the largest metalloproteomes for both Ni and Co.

Bottom Line: 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.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.Our 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Redox Biology Center, University of Nebraska, Lincoln, NE 68588-0664, USA. yzhang@genomics.unl.edu

ABSTRACT

Background: Nickel (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.

Results: We 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.

Conclusion: Our 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.

Show MeSH
Related in: MedlinePlus