Limits...
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.

Show MeSH

Related in: MedlinePlus

Relationship between environmental factors and Ni/Co utilization traits in bacteria. All organisms were classified into four groups: Ni (+), i.e., containing Ni utilization trait; Ni (-), i.e., lacking Ni utilization trait; Co (+), i.e., containing Co utilization trait; Co (-), i.e., lacking Co utilization trait. (A) Habitat; (B) Different host-associated life styles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2667541&req=5

Figure 8: Relationship between environmental factors and Ni/Co utilization traits in bacteria. All organisms were classified into four groups: Ni (+), i.e., containing Ni utilization trait; Ni (-), i.e., lacking Ni utilization trait; Co (+), i.e., containing Co utilization trait; Co (-), i.e., lacking Co utilization trait. (A) Habitat; (B) Different host-associated life styles.

Mentions: Previously we found that habitat, environment and other factors (e.g., oxygen requirement, optimal temperature, optimal pH and GC content) may influence the acquisition/loss of utilization traits of certain trace elements, e.g., selenium (Se) and molybdenum (Mo), in prokaryotes [61,62]. To examine the possibility that Ni and Co utilization may also be affected by some of these factors, we adopted a strategy which was previously used to analyze the evolution of Se and Mo [61,62]. First, similar to Mo utilization [62], we found that the majority of bacteria that utilized neither Ni nor Co were host-associated (i.e., parasites or symbionts, Fig. 8A), implying that host-associated life style may result in the loss of metal utilization, perhaps due to limited space and resources. Considering differences in host-associated conditions (intra- or extracellular) and the relationship between these organisms and their hosts (symbiotic or parasitic), we further divided them into four groups: obligate intracellular symbionts (6 organisms, 2 phyla), extracellular symbionts (19 organisms, 10 phyla), obligate intracellular parasites (35 organisms, 6 phyla) and extracellular parasites (113 organisms, 20 phyla). Interestingly, we found that the majority of intracellular parasites and intracellular symbionts lost the ability to utilize Ni or Co, whereas more than 80% of extracellular symbionts utilized both metals (Fig. 8B). Most obligate intracellular parasites or symbionts had much smaller genomes than extracellular organisms [see Additional file 24]. Thus, it is possible that both metal utilization traits are dispensable for intracellular organisms and hence have been lost due to the pressure on genome size, although these organisms may still depend on host Ni- or Co-dependent proteins. In contrast, the two utilization traits mostly remained intact in essentially all extracellular symbionts, presumably because they are essential to their survival.


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

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

Relationship between environmental factors and Ni/Co utilization traits in bacteria. All organisms were classified into four groups: Ni (+), i.e., containing Ni utilization trait; Ni (-), i.e., lacking Ni utilization trait; Co (+), i.e., containing Co utilization trait; Co (-), i.e., lacking Co utilization trait. (A) Habitat; (B) Different host-associated life styles.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Relationship between environmental factors and Ni/Co utilization traits in bacteria. All organisms were classified into four groups: Ni (+), i.e., containing Ni utilization trait; Ni (-), i.e., lacking Ni utilization trait; Co (+), i.e., containing Co utilization trait; Co (-), i.e., lacking Co utilization trait. (A) Habitat; (B) Different host-associated life styles.
Mentions: Previously we found that habitat, environment and other factors (e.g., oxygen requirement, optimal temperature, optimal pH and GC content) may influence the acquisition/loss of utilization traits of certain trace elements, e.g., selenium (Se) and molybdenum (Mo), in prokaryotes [61,62]. To examine the possibility that Ni and Co utilization may also be affected by some of these factors, we adopted a strategy which was previously used to analyze the evolution of Se and Mo [61,62]. First, similar to Mo utilization [62], we found that the majority of bacteria that utilized neither Ni nor Co were host-associated (i.e., parasites or symbionts, Fig. 8A), implying that host-associated life style may result in the loss of metal utilization, perhaps due to limited space and resources. Considering differences in host-associated conditions (intra- or extracellular) and the relationship between these organisms and their hosts (symbiotic or parasitic), we further divided them into four groups: obligate intracellular symbionts (6 organisms, 2 phyla), extracellular symbionts (19 organisms, 10 phyla), obligate intracellular parasites (35 organisms, 6 phyla) and extracellular parasites (113 organisms, 20 phyla). Interestingly, we found that the majority of intracellular parasites and intracellular symbionts lost the ability to utilize Ni or Co, whereas more than 80% of extracellular symbionts utilized both metals (Fig. 8B). Most obligate intracellular parasites or symbionts had much smaller genomes than extracellular organisms [see Additional file 24]. Thus, it is possible that both metal utilization traits are dispensable for intracellular organisms and hence have been lost due to the pressure on genome size, although these organisms may still depend on host Ni- or Co-dependent proteins. In contrast, the two utilization traits mostly remained intact in essentially all extracellular symbionts, presumably because they are essential to their survival.

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