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Genome and pan-genome analysis of a new exopolysaccharide-producing bacterium Pyschrobacillus sp. isolated from iron ores deposit and insights into iron uptake

Najjari, Afef ; Jabberi, Marwa ; Chérif, Saïda Fatma ; Cherif, Ameur ; Ouzari, Hadda Imene ; Linares-Pastén, Javier A. LU orcid and Sghaier, Haitham (2024) In Frontiers in Microbiology 15.
Abstract
Bacterial exopolysaccharides (EPS) have emerged as one of the key
players in the field of heavy metal-contaminated environmental
bioremediation. This study aimed to characterize and evaluate the metal
biosorption potential of EPS produced by a novel Psychrobacillus
strain, NEAU-3TGS, isolated from an iron ore deposit at Tamra iron mine,
northern Tunisia. Genomic and pan-genomic analysis of NEAU-3TGS
bacterium with nine validated published Psychrobacillus species
was also performed. The results showed that the NEAU-3TGS genome (4.48
Mb) had a mean GC content of 36%, 4,243 coding sequences and 14 RNA
genes. Phylogenomic analysis and calculation of nucleotide identity
(ANI)... (More)
Bacterial exopolysaccharides (EPS) have emerged as one of the key
players in the field of heavy metal-contaminated environmental
bioremediation. This study aimed to characterize and evaluate the metal
biosorption potential of EPS produced by a novel Psychrobacillus
strain, NEAU-3TGS, isolated from an iron ore deposit at Tamra iron mine,
northern Tunisia. Genomic and pan-genomic analysis of NEAU-3TGS
bacterium with nine validated published Psychrobacillus species
was also performed. The results showed that the NEAU-3TGS genome (4.48
Mb) had a mean GC content of 36%, 4,243 coding sequences and 14 RNA
genes. Phylogenomic analysis and calculation of nucleotide identity
(ANI) values (less than 95% for new species with all strains) confirmed
that NEAU-3TGS represents a potential new species. Pangenomic analysis
revealed that Psychrobacillus genomic diversity represents an
“open” pangenome model with 33,091 homologous genes, including 65 core,
3,738 shell, and 29,288 cloud genes. Structural EPS characterization by
attenuated total reflectance-Fourier transform infrared (ATR-FTIR)
spectroscopy showed uronic acid and α-1,4-glycosidic bonds as dominant
components of the EPS. X-ray diffraction (XRD) analysis revealed the
presence of chitin, chitosan, and calcite CaCO3 and confirmed
the amorphous nature of the EPS. Heavy metal bioabsorption assessment
showed that iron and lead were more adsorbed than copper and cadmium.
Notably, the optimum activity was observed at 37°C, pH=7 and after 3 h
contact of EPS with each metal. Genomic insights on iron acquisition and
metabolism in Psychrobacillus sp. NEAU-3TGS suggested that no genes involved in siderophore biosynthesis were found, and only the gene cluster FeuABCD
and trilactone hydrolase genes involved in the uptake of siderophores,
iron transporter and exporter are present. Molecular modelling and
docking of FeuA (protein peptidoglycan siderophore-binding protein) and siderophores ferrienterobactine [Fe+3 (ENT)]-3 and ferribacillibactine [Fe+3 (BB)]-3 ligand revealed that [Fe+3 (ENT)]-3 binds to Phe122, Lys127, Ile100, Gln314, Arg215, Arg217, and Gln252. Almost the same for [Fe+3 (ENT)]-3
in addition to Cys222 and Tyr229, but not Ile100.To the best of our
knowledge, this is the first report on the characterization of EPS and
the adsorption of heavy metals by Psychrobacillus species. The heavy metal removal capabilities may be advantageous for using these organisms in metal remediation. (Less)
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Contribution to journal
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in
Frontiers in Microbiology
volume
15
article number
1440081
pages
17 pages
publisher
Frontiers Media S. A.
ISSN
1664-302X
DOI
10.3389/fmicb.2024.1440081
language
English
LU publication?
yes
id
4f651392-d5af-4d11-9c0d-e4459468b35c
date added to LUP
2024-08-14 00:05:32
date last changed
2024-08-19 12:42:32
@article{4f651392-d5af-4d11-9c0d-e4459468b35c,
  abstract     = {{Bacterial exopolysaccharides (EPS) have emerged as one of the key <br>
players in the field of heavy metal-contaminated environmental <br>
bioremediation. This study aimed to characterize and evaluate the metal <br>
biosorption potential of EPS produced by a novel <i>Psychrobacillus</i> <br>
strain, NEAU-3TGS, isolated from an iron ore deposit at Tamra iron mine,<br>
 northern Tunisia. Genomic and pan-genomic analysis of NEAU-3TGS <br>
bacterium with nine validated published <i>Psychrobacillus</i> species <br>
was also performed. The results showed that the NEAU-3TGS genome (4.48 <br>
Mb) had a mean GC content of 36%, 4,243 coding sequences and 14 RNA <br>
genes. Phylogenomic analysis and calculation of nucleotide identity <br>
(ANI) values (less than 95% for new species with all strains) confirmed <br>
that NEAU-3TGS represents a potential new species. Pangenomic analysis <br>
revealed that <i>Psychrobacillus</i> genomic diversity represents an <br>
“open” pangenome model with 33,091 homologous genes, including 65 core, <br>
3,738 shell, and 29,288 cloud genes. Structural EPS characterization by <br>
attenuated total reflectance-Fourier transform infrared (ATR-FTIR) <br>
spectroscopy showed uronic acid and α-1,4-glycosidic bonds as dominant <br>
components of the EPS. X-ray diffraction (XRD) analysis revealed the <br>
presence of chitin, chitosan, and calcite CaCO<sub>3</sub> and confirmed<br>
 the amorphous nature of the EPS. Heavy metal bioabsorption assessment <br>
showed that iron and lead were more adsorbed than copper and cadmium. <br>
Notably, the optimum activity was observed at 37°C, pH=7 and after 3 h <br>
contact of EPS with each metal. Genomic insights on iron acquisition and<br>
 metabolism in <i>Psychrobacillus</i> sp. NEAU-3TGS suggested that no genes involved in siderophore biosynthesis were found, and only the gene cluster <i>Feu</i>ABCD<br>
 and trilactone hydrolase genes involved in the uptake of siderophores, <br>
iron transporter and exporter are present. Molecular modelling and <br>
docking of <i>Feu</i>A (protein peptidoglycan siderophore-binding protein) and siderophores ferrienterobactine [Fe<sup>+3</sup> (ENT)]<sup>-3</sup> and ferribacillibactine [Fe<sup>+3</sup> (BB)]<sup>-3</sup> ligand revealed that [Fe<sup>+3</sup> (ENT)]<sup>-3</sup> binds to Phe122, Lys127, Ile100, Gln314, Arg215, Arg217, and Gln252. Almost the same for [Fe<sup>+3</sup> (ENT)]<sup>-3</sup><br>
 in addition to Cys222 and Tyr229, but not Ile100.To the best of our <br>
knowledge, this is the first report on the characterization of EPS and <br>
the adsorption of heavy metals by <i>Psychrobacillus</i> species. The heavy metal removal capabilities may be advantageous for using these organisms in metal remediation.}},
  author       = {{Najjari, Afef and Jabberi, Marwa and Chérif, Saïda Fatma and Cherif, Ameur and Ouzari, Hadda Imene and Linares-Pastén, Javier A. and Sghaier, Haitham}},
  issn         = {{1664-302X}},
  language     = {{eng}},
  month        = {{08}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Microbiology}},
  title        = {{Genome and pan-genome analysis of a new exopolysaccharide-producing bacterium <i>Pyschrobacillus sp.</i> isolated from iron ores deposit and insights into iron uptake}},
  url          = {{http://dx.doi.org/10.3389/fmicb.2024.1440081}},
  doi          = {{10.3389/fmicb.2024.1440081}},
  volume       = {{15}},
  year         = {{2024}},
}