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

Abstract

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

Isolation and molecular characterization of Frankia strains resistant to some heavy metals

“…These results are consistent with previous studies shown that the increased concentrations of heavy metals can affect the growth, morphology, and nitrogen fixation activities of soil microorganisms . Resistance of Frankia strains to some heavy metals as Cu, Zn, and Pb at certain concentrations is due to that Frankia strains have proteins for binding and sequestering of heavy metals . In general, the elevated concentrations of these elements are toxic to symbiotic Frankia strains and can affect the structural diversity of soil microorganisms as well .…”

“…It plays an important role in rehabilitation and bioremediation of contaminated soil . It has also been proved that many Frankia strains are able to accumulate and resistant to several toxic metals such as Pb, Cu, and Zn . Furthermore, ability of Frankia to bind and eliminate several toxic heavy metals has been proven .…”

“…Furthermore, ability of Frankia to bind and eliminate several toxic heavy metals has been proven . Furnholm and Tisa showed that each Frankia strain had a special combination of genes for binding, modification, and elimination of heavy metals. Therefore, our study was carried out to isolate different Frankia strains from nodulated Casuarina trees grown in Saudi Arabia and Egypt, as local strains, to be used for soil bioremediation purposes.…”

Solution NMR structure of CHU_1110 from Cytophaga hutchinsonii, an AHSA1 protein potentially involved in metal ion stress response

“…The ArsR family proteins are able to specifically bind to the metal resistance‐related operons and likely dissociate from the operons in the presence of metal ions, permitting the transcription of genes encoding proteins involved in exporting or sequestering the respective ions, a mechanism by which the bacteria can survive under metal surplus conditions . These results of genomic context analysis are consistent with the view of point previously proposed by Furnholm et al They presented that a large group of genes encoding ArsR‐like proteins are individually located in a potential operon with a gene encoding AHSA1 protein, respectively, though a direct link between ArsR and AHSA1 expression has not been elucidated. In the present study, among the 28 proteins with known structures in the AHSA1 family, there are 11 members, like CHU_1110, whose encoding genes are adjacent to and share the same promoter with a gene for ArsR family protein, respectively (Figure B), while other 16 members do not possess corresponding genomic context.…”

Genome Sequence of Frankia sp. Strain CH37, a Metallophore-Producing, Nitrogen-Fixing Actinobacterium Isolated from the Sea Buckthorn, Hippophae rhamnoides (Elaeagnaceae)

“…Metallophores are a unique class of organic ligands released into the environment for multiple functions in metal management, such as metal acquisition and detoxification ( 12 – 15 ). Sequencing the genome of this strain was required to shed light upon metallophore biosynthetic genes and gene clusters that might be involved in metal homeostasis ( 16 ), metal detoxification of, e.g., copper ( 17 ), and plant- Frankia interactions ( 8 ).…”