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The ins and outs of metal homeostasis by the root nodule actinobacterium Frankia

Identifieur interne : 000124 ( Main/Exploration ); précédent : 000123; suivant : 000125

The ins and outs of metal homeostasis by the root nodule actinobacterium Frankia

Auteurs : Teal R. Furnholm [États-Unis] ; Louis S. Tisa [États-Unis]

Source :

RBID : PMC:4531530

Abstract

Background

Frankia are actinobacteria that form a symbiotic nitrogen-fixing association with actinorhizal plants, and play a significant role in actinorhizal plant colonization of metal contaminated areas. Many Frankia strains are known to be resistant to several toxic metals and metalloids including Pb2+, Al+3, SeO2, Cu2+, AsO4, and Zn2+. With the availability of eight Frankia genome databases, comparative genomics approaches employing phylogeny, amino acid composition analysis, and synteny were used to identify metal homeostasis mechanisms in eight Frankia strains. Characterized genes from the literature and a meta-analysis of 18 heavy metal gene microarray studies were used for comparison.

Results

Unlike most bacteria, Frankia utilize all of the essential trace elements (Ni, Co, Cu, Se, Mo, B, Zn, Fe, and Mn) and have a comparatively high percentage of metalloproteins, particularly in the more metal resistant strains. Cation diffusion facilitators, being one of the few known metal resistance mechanisms found in the Frankia genomes, were strong candidates for general divalent metal resistance in all of the Frankia strains. Gene duplication and amino acid substitutions that enhanced the metal affinity of CopA and CopCD proteins may be responsible for the copper resistance found in some Frankia strains. CopA and a new potential metal transporter, DUF347, may be involved in the particularly high lead tolerance in Frankia. Selenite resistance involved an alternate sulfur importer (CysPUWA) that prevents sulfur starvation, and reductases to produce elemental selenium. The pattern of arsenate, but not arsenite, resistance was achieved by Frankia using the novel arsenite exporter (AqpS) previously identified in the nitrogen-fixing plant symbiont Sinorhizobium meliloti. Based on the presence of multiple tellurite resistance factors, a new metal resistance (tellurite) was identified and confirmed in Frankia.

Conclusions

Each strain had a unique combination of metal import, binding, modification, and export genes that explain differences in patterns of metal resistance between strains. Frankia has achieved similar levels of metal and metalloid resistance as bacteria from highly metal-contaminated sites. From a bioremediation standpoint, it is important to understand mechanisms that allow the endosymbiont to survive and infect actinorhizal plants in metal contaminated soils.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1092) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/1471-2164-15-1092
PubMed: 25495525
PubMed Central: 4531530


Affiliations:


Links toward previous steps (curation, corpus...)


Le document en format XML

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<sec>
<title>Background</title>
<p>
<italic>Frankia</italic>
are actinobacteria that form a symbiotic nitrogen-fixing association with actinorhizal plants, and play a significant role in actinorhizal plant colonization of metal contaminated areas. Many
<italic>Frankia</italic>
strains are known to be resistant to several toxic metals and metalloids including Pb
<sup>2+</sup>
, Al
<sup>+3</sup>
, SeO
<sub>2</sub>
, Cu
<sup>2+</sup>
, AsO
<sub>4</sub>
, and Zn
<sup>2+</sup>
. With the availability of eight
<italic>Frankia</italic>
genome databases, comparative genomics approaches employing phylogeny, amino acid composition analysis, and synteny were used to identify metal homeostasis mechanisms in eight
<italic>Frankia</italic>
strains. Characterized genes from the literature and a meta-analysis of 18 heavy metal gene microarray studies were used for comparison.</p>
</sec>
<sec>
<title>Results</title>
<p>Unlike most bacteria,
<italic>Frankia</italic>
utilize all of the essential trace elements (Ni, Co, Cu, Se, Mo, B, Zn, Fe, and Mn) and have a comparatively high percentage of metalloproteins, particularly in the more metal resistant strains. Cation diffusion facilitators, being one of the few known metal resistance mechanisms found in the
<italic>Frankia</italic>
genomes, were strong candidates for general divalent metal resistance in all of the
<italic>Frankia</italic>
strains. Gene duplication and amino acid substitutions that enhanced the metal affinity of CopA and CopCD proteins may be responsible for the copper resistance found in some
<italic>Frankia</italic>
strains. CopA and a new potential metal transporter, DUF347, may be involved in the particularly high lead tolerance in
<italic>Frankia</italic>
. Selenite resistance involved an alternate sulfur importer (CysPUWA) that prevents sulfur starvation, and reductases to produce elemental selenium. The pattern of arsenate, but not arsenite, resistance was achieved by
<italic>Frankia</italic>
using the novel arsenite exporter (AqpS) previously identified in the nitrogen-fixing plant symbiont
<italic>Sinorhizobium meliloti</italic>
. Based on the presence of multiple tellurite resistance factors, a new metal resistance (tellurite) was identified and confirmed in
<italic>Frankia</italic>
.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Each strain had a unique combination of metal import, binding, modification, and export genes that explain differences in patterns of metal resistance between strains.
<italic>Frankia</italic>
has achieved similar levels of metal and metalloid resistance as bacteria from highly metal-contaminated sites. From a bioremediation standpoint, it is important to understand mechanisms that allow the endosymbiont to survive and infect actinorhizal plants in metal contaminated soils.</p>
</sec>
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<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/1471-2164-15-1092) contains supplementary material, which is available to authorized users.</p>
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<author>
<name sortKey="Ball, Ca" uniqKey="Ball C">CA Ball</name>
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<author>
<name sortKey="Blake, Ja" uniqKey="Blake J">JA Blake</name>
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<name sortKey="Botstein, D" uniqKey="Botstein D">D Botstein</name>
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<name sortKey="Butler, H" uniqKey="Butler H">H Butler</name>
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<author>
<name sortKey="Cherry, Jm" uniqKey="Cherry J">JM Cherry</name>
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<author>
<name sortKey="Sherlock, G" uniqKey="Sherlock G">G Sherlock</name>
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<name sortKey="Galperin, My" uniqKey="Galperin M">MY Galperin</name>
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<name sortKey="Natale, Da" uniqKey="Natale D">DA Natale</name>
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<name sortKey="Koonin, Ev" uniqKey="Koonin E">EV Koonin</name>
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<name sortKey="Kumar, S" uniqKey="Kumar S">S Kumar</name>
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<author>
<name sortKey="Nei, M" uniqKey="Nei M">M Nei</name>
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<author>
<name sortKey="Dudley, J" uniqKey="Dudley J">J Dudley</name>
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