The Development of Bacteriophage Resistance in Vibrio alginolyticus Depends on a Complex Metabolic Adaptation Strategy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Vibrio alginolyticus Strain V1
2.2. Bacteriophages Aphrodite1, phiSt2, and Ares1
2.3. Vibrio alginolyticus Phage-Resistant Strains
2.4. Growth Kinetics, Phage Biological Characteristics, and Phage Adsorption Dynamics
2.5. Phage DNA Extraction and Sequencing
2.6. Bacterial DNA Extraction and Sequencing
2.7. Bacteria and Bacteriophage Genome Analyses
2.8. Gene Expression Analysis
2.9. Metabolite Extraction and Intracellular Metabolite Analysis
2.10. Statistical Analysis
2.11. Accession Numbers
3. Results
3.1. Description of Novel Bacteriophage Isolates
3.2. Cross Infection and Growth Curve of Phage-Resistant Strains
3.3. Study of Anti-Phage Defense Systems of Vibrio alginolyticius
3.4. Transcript Profiling of Bacterial Genes Involved in the Phage Infection Process
3.5. Transcript Profiling of Genes Coding for Key Metabolic Enzymes
3.6. Metabolomic Profiling of the Resistant Strains
3.7. Comparative Genomic Analysis of Resistant Vibrio Strains
4. Discussion
4.1. Major Transcriptional Reprogramming Could Confer Phage Tolerance
4.2. Resistance to Lytic Bacteriophages Includes Metabolic Adaptation Mechanisms
4.3. Transcription Reprogramming in Phage-Resistant Becterial Strains Could Be Triggered by Genomic Lesions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Phage | Family | Genus | Lifestyle | Genome (bps) | GC % | Predicted # ORFs | Latent Period | Accession Number | Reference |
---|---|---|---|---|---|---|---|---|---|
Aphrodite1 | Myoviridae | Aphroditevirus | Lytic | 237.722 | 43.4 | 207 | 80 min | MG720308 | This study |
phiSt2 | Myoviridae | Schizotequatrovirus | Lytic | 250.485 | 42.6 | 412 | 30 min | KT919973 | [30,31] |
Ares1 | Siphoviridae | unclassified | Unknown | 80.500 | 45.1 | 119 | 30 min | MG720309 | This study |
Bacteriophages with High Lytic Activity | |||
---|---|---|---|
Vibrio alginolyticus Strains | Aphrodite1 | phiSt2 | Ares1 |
Control (wild type) | + | + | + |
VaAphrodite1 | - | + | - |
VaphiSt2 | + | - | + |
VaAres1 | + | + | - |
Gene Name | Nutrient Transport Participation | Type of Transporter | Subunit | Subunit Role |
---|---|---|---|---|
mtlA | Mannitol | PTS | IIA, IIB, IIC | Affinity, Transport, Energy |
treB | Trehalose | PTS | IIB, IIC | Affinity, Transport |
fruA | Fructose | PTS | IIB, IIC | Affinity, Transport |
celB | Cellulose | PTS | IIC | Affinity |
ptsG 1 | Glucose | PTS | IIB, IIC | Affinity, Transport |
ptsG 2 | Glucose | PTS | IIB, IIC | Affinity, Transport |
crr | Glucose | PTS | IIB, IIC | Energy |
ptsN | Nitrogen | PTS | IIA | Transport |
ptsH | Phosphorus | PTS | IIA | Transport |
tyrP | Tyrosine | - | - | |
rbsA | Ribose | ABC | ATP-subunit | Energy |
metQ | Methionine | ABC | IIA | Affinity |
metl | Methionine | ABC | Substrate subunit | Transport |
metN | Methionine | ABC | Transmembrane subunit | Energy |
artP | Arginine | ABC | Substrate subunit | Affinity |
artL | Arginine | ABC | ATP-subunit | Energy |
tcyP | Cysteine | - | - | Transport |
lysE | Lysine | LysE-like | - | Lysine Export |
rhtB 1 | Homoserine and Threonine | LysE-like | - | Homoserine and Threonine Export |
rhtB 2 | Homoserine and Threonine | LysE-like | - | Homoserine and Threonine Export |
hisP | Lysine, Histidine, Arginine, Ornithine | ABC | ATP-subunit | Energy |
azlC 1 | Valine, Isoleucine, Leucine | ABC | Transmembrane subunit | Transport |
azlC 2 | Valine, Isoleucine, Leucine | ABC | Transmembrane subunit | Transport |
livH | Valine, Isoleucine, Leucine | ABC | Transmembrane subunit | Transport |
livM | Valine, Isoleucine, Leucine | ABC | Transmembrane subunit | Transport |
Expression Ratio vs. Control | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Gene | VaAphrodite1 | VaphiSt2 | VaAres1 | |||||||
livH | * | * | * | |||||||
livB | * | * | * | |||||||
metl | * | * | ||||||||
metN | * | * | ||||||||
metQ | * | |||||||||
tcyp | * | * | * | |||||||
lysE | * | |||||||||
hisp | * | * | ||||||||
ptsG1 | * | |||||||||
ptsG2 | * | * | ||||||||
crr | * | * | ||||||||
rbsH | * | * | ||||||||
cellB | * | * | ||||||||
ptsH | * | |||||||||
murE | * | |||||||||
gltA | * | |||||||||
frd | * | * | ||||||||
mdh1 | * | * | ||||||||
pykA | * | |||||||||
pykF | ||||||||||
pckA | * | * | ||||||||
r > 10 | 4 < r < 10 | 2 < r < 4 | 1.41 < r < 2 | 1.19 < r < 1.41 | 0.84 < r < 1.19 | 0.71 < r < 0.84 | 0.5 < r < 0.71 | 0.25 < r < 0.5 | 0.1 < r < 0.25 | r < 0.1 |
Gene Name | Coding Enzyme | E.C. Number | Metabolic Pathway |
---|---|---|---|
ald | Alanine dehydrogenase | 1.4.11 | Alanine metabolism |
agxT | Alanine-glycosylate and serine pyruvate aminotransferase | 2.6.1.44 | Alanine metabolism |
panD | aspartate 4-decarboxylase; desulfinase | 4.1.1.12 | Alanine metabolism |
lysA 1 | Lysine decarboxylase | 4.1.1.20 | Lysine metabolism |
lysA 2 | Lysine decarboxylase | 4.1.1.20 | Lysine metabolism |
murE | Amino acid ligase | 6.3.2.13 | Peptidoglycan biosynthesis |
gltA | Citrate synthase | 2.3.3.16 | TCA cycle |
mdh 1 | Malic acid decarboxylase | 1.1.1.37 | TCA cycle |
frd | Fumarate reductase | 1.3.5.4 | TCA cycle |
pykA | Pyruvate kinase | 2.7.1.40 | Anaplerotic reactions of the TCA cycle |
pykF | Pyruvate kinase | 2.7.1.40 | Anaplerotic reactions of the TCA cycle |
pckA | PEP carboxykinase | 4.1.1.49 | Anaplerotic reactions of the TCA cycle |
mdh 2 | Malic acid dehydrogenase | 1.1.1.38 | Anaplerotic reactions of the TCA cycle |
mdh 3 | Malic acid dehydrogenase | 1.1.1.39 | Anaplerotic reactions of the TCA cycle |
ppc | PEP carboxylase | 4.1.1.31 | Anaplerotic reactions of the TCA cycle |
Compound | RT | M/Z | Control | VaAphrodite1 | VaphiSt2 | VaAres1 | p |
---|---|---|---|---|---|---|---|
Phenylalanine | 25.90 | 218 | 0.046 | 0.068 | 0.079 | 0.087 | 0.093 |
Lysine | 32.19 | 73 | 0.037 | 0.053 | 0.558 | 0.025 | 0.000 |
Isoleucine | 17.34 | 158 | 0.074 | 0.091 | 0.113 | 0.105 | 0.129 |
Alanine | 12.05 | 116 | 0.246 | 0.184 | 0.304 | 0.440 | 0.000 |
Ornithine | 30.02 | 142 | 0.024 | 0.127 | 0.080 | 0.000 | 0.000 |
Proline | 17.54 | 142 | 0.059 | 0.000 | 0.057 | 0.072 | 0.000 |
Valine | 15.19 | 144 | 0.121 | 0.170 | 0.183 | 0.174 | 0.243 |
Glycine | 17.73 | 174 | 0.084 | 0.157 | 0.121 | 0.219 | 0.032 |
Leucine | 16.73 | 158 | 0.161 | 0.239 | 0.376 | 0.532 | 0.002 |
Aspartic acid | 23.21 | 232 | 0.086 | 0.000 | 0.071 | 0.073 | 0.000 |
Glutamic acid | 25.61 | 246 | 0.248 | 0.116 | 0.486 | 0.343 | 0.000 |
Pyroglutamic acid | 23.37 | 156 | 0.121 | 0.092 | 0.239 | 0.156 | 0.001 |
Norleucine | 16.73 | 158 | 0.178 | 0.238 | 0.324 | 0.347 | 0.047 |
Putrescine | 28.39 | 174 | 0.166 | 0.121 | 0.268 | 0.201 | 0.000 |
Cadaverine | 30.52 | 174 | 0.717 | 1.120 | 0.361 | 0.507 | 0.000 |
Succinic acid | 17.92 | 148 | 1.394 | 1.271 | 1.784 | 2.881 | 0.003 |
Pipecolic acid | 23.37 | 156 | 0.000 | 0.074 | 0.000 | 0.000 | 0.000 |
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Skliros, D.; Kalatzis, P.G.; Kalloniati, C.; Komaitis, F.; Papathanasiou, S.; Kouri, E.D.; Udvardi, M.K.; Kokkari, C.; Katharios, P.; Flemetakis, E. The Development of Bacteriophage Resistance in Vibrio alginolyticus Depends on a Complex Metabolic Adaptation Strategy. Viruses 2021, 13, 656. https://doi.org/10.3390/v13040656
Skliros D, Kalatzis PG, Kalloniati C, Komaitis F, Papathanasiou S, Kouri ED, Udvardi MK, Kokkari C, Katharios P, Flemetakis E. The Development of Bacteriophage Resistance in Vibrio alginolyticus Depends on a Complex Metabolic Adaptation Strategy. Viruses. 2021; 13(4):656. https://doi.org/10.3390/v13040656
Chicago/Turabian StyleSkliros, Dimitrios, Panos G. Kalatzis, Chrysanthi Kalloniati, Fotios Komaitis, Sokratis Papathanasiou, Evangelia D. Kouri, Michael K. Udvardi, Constantina Kokkari, Pantelis Katharios, and Emmanouil Flemetakis. 2021. "The Development of Bacteriophage Resistance in Vibrio alginolyticus Depends on a Complex Metabolic Adaptation Strategy" Viruses 13, no. 4: 656. https://doi.org/10.3390/v13040656