Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains, Plasmids, and Culture Conditions
2.2. PCR Assays
2.3. Genome Sequencing
2.4. Construction of a scrA Mutant in Pdd DK32
2.5. Growth Assays with Sucrose as a Carbon Source
2.6. Construction of a Transcriptional Fusion of scrA Promoter to a lacZ Reporter Gene, and β-Galactosidase Assays
2.7. Comparative Genomics and Molecular Phylogeny Analyses
2.8. Database Submission
3. Results
3.1. Identification of Two Different Genetic Variants of a Four Gene Cluster Encoding Functions for Sucrose Uptake and Catabolism in Pdd Strains
3.2. Deletion of scrA in the scr+ Strain DK32 Causes Green Colonies on TCBS Medium, and Abolishes Growth with Sucrose as Carbon Source
3.3. Scr Clusters Are Inserted into Putative Hot-Spots for DNA Acquisition in Pdd Genomes
3.4. Scr Clusters Occur in Different Genetic Lineages of Pdd
3.5. Incongruences between the Species Tree and the Sucrose Genes Tree Reveal Extensive Horizontal Transfer of scr Genes among Species of Vibrio and Photobacterium
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Strain | Isolation Source | Strain Reference | Scr Phenotype a | Presence of Sucrose Genes b | Genbank Acc. No. c | Genome Reference |
---|---|---|---|---|---|---|
154dp-OG1 | European sea bass, Turkey | [30] | − | − | NA | NA |
164dp-OG2 | European sea bass, Turkey | [30] | − | − | VAUU00000000 | [26] |
144bp-OG3 | European sea bass, Turkey | [30] | − | − | VAND00000000 | [26] |
162bp-OG4A | European sea bass, Turkey | [30] | + | + | JABWTP000000000 | This study |
158dp-OG5 | European sea bass, Turkey | [30] | − | − | NA | NA |
189bp-OG7B | European sea bass, Turkey | [30] | + | + | JABXOP000000000 | This study |
82dy-OG8 | European sea bass, Turkey | [30] | − | − | JABXOQ000000000 | This study |
64bp-OG9 | European sea bass, Turkey | [30] | + | + | VANE00000000 | [26] |
156dp-OG10A | European sea bass, Turkey | [30] | − | − | NA | NA |
125dy-OG11 | European sea bass, Turkey | [30] | + | + | JACFTX000000000 | This study |
70dps-OG12 | European sea bass, Turkey | [30] | + | + | VANF00000000 | [26] |
164dpbuy-OG13B | European sea bass, Turkey | [30] | − | − | NA | NA |
111bp-OG15A | European sea bass, Turkey | [30] | − | − | VANG00000000 | [26] |
89dp-OG16 | European sea bass, Turkey | [30] | + | + | VANH00000000 | [26] |
CIP 102761 | Damselfish, United Estates | [32] | − | − | ADBS00000000 | Unpublished |
TW250/03 | Gilthead seabream | Laboratory collection | + | + | JABXOR000000000 | This study |
RM-71 | Turbot, Spain | [33] | − | − | LYBT00000000 | [34] |
A-162 | Eel, Belgium | NA | − | − | LZFN00000000 | [34] |
LD-07 | Gilthead seabream, Spain | [35] | − | − | LYBU00000000 | [34] |
DK2 | Rainbow trout, Denmark | [24,36] | − | − | PVXF00000000 | [24] |
DK3 | Rainbow trout, Denmark | [24,36] | − | − | PVXG00000000 | [24] |
DK20 | Rainbow trout, Denmark | [24,37] | − | − | PVXH00000000 | [24] |
DK29 | Rainbow trout, Denmark | [24,37] | − | − | PVXI00000000 | [24] |
DK32 | Rainbow trout, Denmark | [24,37] | + | + | JABWTO000000000 | This study |
CDC-1421-81 | Fish, Senegal | [38] | − | − | JABXYE000000000 | This study |
RG-191 | Turbot, Spain | [33] | − | − | NA | NA |
ATCC35083 | Brown shark, United States | [39] | − | − | NA | NA |
CDC-2227-81 | Human, United States | [38] | − | − | VZUQ00000000 | [40] |
80077637 | Human, Australia | [23] | − | − | WAEO00000000 | [40] |
ACRP-72.1 | Turbot, Portugal | Laboratory collection | − | − | NA | NA |
DLC 1.2 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
DLC 4.1 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
DLC 7.1 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
DLC 7.3 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
DLC 8.1 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
DLC 9.1 | Gilthead seabream, Spain | Laboratory collection | − | − | NA | NA |
Strain or Plasmid | Description a | Reference/Source |
---|---|---|
Strains | ||
P. damselae subsp. damselae | ||
DK32 | Isolated from rainbow trout; ferments sucrose (Scr+) | [24,37] |
SSS165 | DK32 ΔscrA. Does not ferment sucrose (Scr−) | This study |
SSS250 | DK32 with plasmid pSSS250 | This study |
E. coli | ||
DH5α | Cloning strain | Laboratory stock |
S17-1-λpir | RP4-2(Km::Tn7, Tc::Mu-1) pro-82 λpir recA1 endA1 thiE1 hsdR17 creC510 | [41] |
Plasmids | ||
pHRP309 | lacZ reporter plasmid, mob Gmr | [42] |
pSSS250 | pHRP309 with a transcriptional fusion of scrA promoter to lacZ | This study |
pWKS30 | Low-copy-number cloning vector; Apr | [43] |
pNidKan | Suicide vector derived from pCVD442; Kmr | [44] |
Name of Primer Pair | Oligonucleotide Sequence 1 | Amplicon Size (bp) |
---|---|---|
scrA-1-2 | F: 5’-GCTCTAGAGCCATTCGCACAACACTTTG-3’ R: 5’-GCGGATCCGTTCGCTAGATCAGTCAATC-3’ | 2106 |
scrA-3-4 | F: 5’-GCGGATCCTCAAGGTGCTGCCGCTTTAG-3’ R: 5’-GCGAATTCAGGACCTTTATGCTGCCACG-3’ | 2122 |
scrA-mutant-test | F: 5’-GGCTCAGGCATAGTAAACCA-3’ R: 5’-CCGCGATAAATGGGTAACGT-3’ | 1024 |
scrA-promoter | F: 5’-GCTCTAGAACATCATGCAGACTCGCCAT-3’ R: 5’-GCGGATCCCTCTTTAGCTACTGCCGGAT-3’ | 281 |
scrK | F: 5’-TTACGCGACTCACCTCGACA-3’ R: 5’-ATCGGTCGCGCAGAACAAAC-3’ | 373 |
scrB | F: 5’-GACCAAGACTACGATTCACA-3’ R: 5’-ACACTCCCACATGTACCCAA-3’ | 372 |
Species | Accession Number |
---|---|
Vibrio alfacsensis | CP032093.1 |
V. parahaemolyticus | QPIY01000005 |
V. alginolyticus | AAPS01000004 |
Vibrio rotiferianus | NZ_KV861318 |
Vibrio diabolicus | CP014133 |
Vibrio harveyi | CP014038 |
Vibrio fortis | NZ_JFFR01000009 |
Vibrio cyclitrophicus | VUKB01000001 |
Photobacterium lutimaris | NZ_SNZO01000003 |
Vibrio crassostreae | NZ_AJZB02000137 |
Photobacterium angustum | NZ_PYOK01000006 |
Photobacterium frigidiphilum | NZ_PYMJ01000001 |
Photobacterium profundum | NZ_PYOD01000001 |
Photobacterium indicum | NZ_PYOC01000002 |
V. cholerae | NZ_VTLI01000001 |
Photobacterium halotolerans | NZ_AULG01000013 |
Photobacterium rosenbergii | NZ_PYMB01000001 |
Photobacterium lipolyticum | NZ_PYMC01000002 |
Attribute | 162bp-OG4A (Scr+) | 189bp-OG7B (Scr+) | 82dy-OG8 (Scr−) | 125dy-OG11 (Scr+) | DK32 (Scr+) | TW250/03 (Scr+) | CDC-1421-81 (Scr−) |
---|---|---|---|---|---|---|---|
Accession no. | JABWTP000000000 | JABXOP000000000 | JABXOQ000000000 | JACFTX000000000 | JABWTO000000000 | JABXOR000000000 | JABXYE000000000 |
Genome size (bp) | 4,306,101 bp | 4,302,857 bp | 4,627,325 bp | 4,450,948 bp | 4,248,331 bp | 4,695,503 bp | 4,432,211 bp |
Contigs | 133 | 127 | 138 | 147 | 106 | 1649 | 81 |
% GC | 40.70% | 40.70% | 40.70% | 40.70% | 40.60% | 39.80% | 40.40% |
Genes (total) | 3809 | 3807 | 4096 | 4089 | 3750 | 5089 | 3916 |
CDSs | 3756 | 3758 | 4038 | 3879 | 3699 | 5041 | 3860 |
Strain | 162bp-OG4A | 189bp-OG7B | 64bp-OG9 | 125dy-OG11 | 70dps-OG12 | 89dp-OG16 | DK32 | TW250/03 |
---|---|---|---|---|---|---|---|---|
Accession no. | JABWTP000000000 | JABXOP000000000 | VANE00000000 | JACFTX000000000 | VANF00000000 | VANH00000000 | JABWTO000000000 | JABXOR000000000 |
Sucrose operon genes (locus_tag) | ||||||||
scrA | HU985_14400 | HVV26_09235 | FD719_10830 | H3N34_00965 | FD720_04185 | FD722_11585 | HU831_00535 | HWA77_17195 |
scrB | HU985_14390 | HVV26_09225 | FD719_10820 | H3N34_00955 | FD720_04175 | FD722_11575 | HU831_00545 | HWA77_17185 |
scrK | HU985_14395 | HVV26_09230 | FD719_10825 | H3N34_00960 | FD720_04180 | FD722_11580 | HU831_00540 | HWA77_17190 |
scrR | HU985_14405 | HVV26_09240 | FD719_10835 | H3N34_00970 | FD720_04190 | FD722_11590 | HU831_00530 | HWA77_17200 |
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Abushattal, S.; Vences, A.; Barca, A.V.; Osorio, C.R. Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae. Genes 2020, 11, 1244. https://doi.org/10.3390/genes11111244
Abushattal S, Vences A, Barca AV, Osorio CR. Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae. Genes. 2020; 11(11):1244. https://doi.org/10.3390/genes11111244
Chicago/Turabian StyleAbushattal, Saqr, Ana Vences, Alba V. Barca, and Carlos R. Osorio. 2020. "Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae" Genes 11, no. 11: 1244. https://doi.org/10.3390/genes11111244