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Isolation and characterization of novel Fusobacterium nucleatum bacteriophages

Wang, Yue, Liu, Zhitong, Chen, Qian, Yi, Liqi, Xu, Zihao, Cai, Mufeng, Qin, Jinhong, Zhang, Yan, Du, Guanhuan, Hong, Jie, Guo, Xiaokui, Liu, Chang·2022·Frontiers in Microbiology
DOI 10.3389/fmicb.2022.945315PMC PMC9670143
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Abstract

Fusobacterium nucleatum is a strictly anaerobic, Gram-negative bacterial species that is a member of the commensal flora in the oral cavity and gut. Recent studies suggested that the increase of abundance is associated with the development of various diseases, among which colorectal cancer is of the biggest concerns. Phage therapy is regarded as a potential approach to control the number of F. nucleatum, which may contribute to the prevention and treatment of related diseases. In this study, we isolated five isolates of bacteriophage targeting F. nucleatum. The morphological, biological, genomic and functional characteristics of five bacteriophages were investigated. Transmission electron microscopy revealed that JD-Fnp1 ~ JD-Fnp5 are all myoviruses. The size of the JD-Fnp1 ~ JD-Fnp5 genomes was 180,066 bp (JD-Fnp1), 41,329 bp (JD-Fnp2), 38,962 bp (JD-Fnp3), 180,231 bp (JD-Fnp4), and 41,353 bp (JD-Fnp5) respectively. The biological features including pH and heat stability, host range, growth characteristics of JD-Fnp1 ~ JD-Fnp5 displayed different patterns. Among them, JD-Fnp4 is considered to have the greatest clinical application value. The identification and characterization of JD-Fnp1 ~ JD-Fnp5 provides a basis for subsequent therapeutic strategy exploration of F. nucleatum-related diseases.

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Figure 1 TEM micrograph of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1. The length and width of the head are 155 ± 5 nm and 140 ± 5 nm respectively, and the length of its retractable tail is 335 ± 5 nm. Magnification: × 36 k. (B) JD-Fnp2. The length of its head is 60 ± 2 nm, and the width is 50 ± 3 nm. The retractable tail is 130 ± 5 nm in length. Magnification: × 73 k. (C) JD-Fnp3. It has a head of the polyhedron with a radial length of 55 ± 3 nm, and a retractable tail with a length of 135 ± 2 nm. Magnification: × 54 k. (D) JD-Fnp4. The diameter of the capsid head and the length of the flexible tail are about 130 ± 5 nm and 300 ± 4 nm. Magnification: × 98 k. (E) JD-Fnp5. The diameter of the capsid head and the length of the flexible tail are 61 ± 2 nm and 144 ± 5 nm. Magnification: × 150 k. These measurements were taken on 10 different particles.
Figure 1 TEM micrograph of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1. The length and width of the head are 155 ± 5 nm and 140 ± 5 nm respectively, and the length of its retractable tail is 335 ± 5 nm. Magnification: × 36 k. (B) JD-Fnp2. The length of its head is 60 ± 2 nm, and the width is 50 ± 3 nm. The retractable tail is 130 ± 5 nm in length. Magnification: × 73 k. (C) JD-Fnp3. It has a head of the polyhedron with a radial length of 55 ± 3 nm, and a retractable tail with a length of 135 ± 2 nm. Magnification: × 54 k. (D) JD-Fnp4. The diameter of the capsid head and the length of the flexible tail are about 130 ± 5 nm and 300 ± 4 nm. Magnification: × 98 k. (E) JD-Fnp5. The diameter of the capsid head and the length of the flexible tail are 61 ± 2 nm and 144 ± 5 nm. Magnification: × 150 k. These measurements were taken on 10 different particles.CC BY · PubMed Central
Figure 2 The adsorption profile of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis shows the incubation time of phages with host bacteria, and the y-axis shows the percentage of free phage particles. Data are from three times independent experiments.
Figure 2 The adsorption profile of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis shows the incubation time of phages with host bacteria, and the y-axis shows the percentage of free phage particles. Data are from three times independent experiments.CC BY · PubMed Central
Figure 3 The one-step growth profile of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis shows the incubation time of phages with host bacteria; the y-axis shows the fold of increase of phage titers at different time points. Data are from three times independent experiments.
Figure 3 The one-step growth profile of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis shows the incubation time of phages with host bacteria; the y-axis shows the fold of increase of phage titers at different time points. Data are from three times independent experiments.CC BY · PubMed Central
Figure 4 Thermal stability of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis represents temperature range; the y-axis represents the relative titer of JD-Fnp phage to the titer at 37°C or 4°C (The control temperature of JD-Fnp1 ~ JD-Fnp4 is 37°C, and the control temperature of JD-Fnp5 is 4°C that the phage has the best stability); Percentage of active JD-Fnp phages = (N/N0) × 100, where N is the number of viable phages after 1 h of incubation and N0 was the initial number of phages. All experiments were repeated in triplicate.
Figure 4 Thermal stability of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis represents temperature range; the y-axis represents the relative titer of JD-Fnp phage to the titer at 37°C or 4°C (The control temperature of JD-Fnp1 ~ JD-Fnp4 is 37°C, and the control temperature of JD-Fnp5 is 4°C that the phage has the best stability); Percentage of active JD-Fnp phages = (N/N0) × 100, where N is the number of viable phages after 1 h of incubation and N0 was the initial number of phages. All experiments were repeated in triplicate.CC BY · PubMed Central
Figure 5 pH stability of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis represents the pH range; the y-axis shows the percentage of the active phage titers in different pH values to that in pH 7.5. All experiments were repeated in triplicate.
Figure 5 pH stability of phages JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. The x-axis represents the pH range; the y-axis shows the percentage of the active phage titers in different pH values to that in pH 7.5. All experiments were repeated in triplicate.CC BY · PubMed Central
Figure 6 In vitro bactericidal activity of JD-Fnp1 ~ JD-Fnp5 with host bacteria JD-Fn1. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. F. nucleatum strain JD-Fn1 was infected by JD-Fnp phages with different MOI. The x-axis represents the co-culture time of JD-Fnp phage and JD-Fn1; the y-axis represents the change of OD600 in the mixture. Data are displayed as the means ± SD (error bars) from three independent experiments.
Figure 6 In vitro bactericidal activity of JD-Fnp1 ~ JD-Fnp5 with host bacteria JD-Fn1. (A) JD-Fnp1; (B) JD-Fnp2; (C) JD-Fnp3; (D) JD-Fnp4; (E) JD-Fnp5. F. nucleatum strain JD-Fn1 was infected by JD-Fnp phages with different MOI. The x-axis represents the co-culture time of JD-Fnp phage and JD-Fn1; the y-axis represents the change of OD600 in the mixture. Data are displayed as the means ± SD (error bars) from three independent experiments.CC BY · PubMed Central
Figure 7 Complete genome sequences of JD-Fnp1 ~ JD-Fnp5. The functional modules were assigned based on gene annotation and genomic organization and are shown in different colors.
Figure 7 Complete genome sequences of JD-Fnp1 ~ JD-Fnp5. The functional modules were assigned based on gene annotation and genomic organization and are shown in different colors.CC BY · PubMed Central
Figure 8 Comparative genomic analysis of JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1 and JD-Fnp4; (B) JD-Fnp2, JD-Fnp3 and JD-Fnp5. Analysis was performed with blastn (BLAST v2.2.31+) at DNA level. The nucleotide identity of the homologous regions (percentage) is shown as a color gradient, the pink bar represents for forward blast hits and the gray bar represents for inverted blast hits; the scale is shown below. Known functional homologous genes are shown below.
Figure 8 Comparative genomic analysis of JD-Fnp1 ~ JD-Fnp5. (A) JD-Fnp1 and JD-Fnp4; (B) JD-Fnp2, JD-Fnp3 and JD-Fnp5. Analysis was performed with blastn (BLAST v2.2.31+) at DNA level. The nucleotide identity of the homologous regions (percentage) is shown as a color gradient, the pink bar represents for forward blast hits and the gray bar represents for inverted blast hits; the scale is shown below. Known functional homologous genes are shown below.CC BY · PubMed Central
Figure 9 Phylogenetic tree of JD-Fnp1 ~ JD-Fnp5 and relative bacteriophages based on the complete genome sequences. The genome sequences of two F. nucleatum phages reported previously were downloaded from NCBI, and all the accession numbers are shown in () following the names of phages. The phylogenetic tree was constructed with VipTree (http://www.genome.jp/viptree) based on whole genome sequences at DNA level.
Figure 9 Phylogenetic tree of JD-Fnp1 ~ JD-Fnp5 and relative bacteriophages based on the complete genome sequences. The genome sequences of two F. nucleatum phages reported previously were downloaded from NCBI, and all the accession numbers are shown in () following the names of phages. The phylogenetic tree was constructed with VipTree (http://www.genome.jp/viptree) based on whole genome sequences at DNA level.CC BY · PubMed Central

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Metadata

Authors
Wang, Y., Liu, Z., Chen, Q., Yi, L., Xu, Z., Cai, M., Qin, J., Zhang, Y., Du, G., Hong, J., Guo, X., & Liu, C.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2022-11-03
Volume
13
ISSN
1664-302X
DOI
10.3389/fmicb.2022.945315
PMC
PMC9670143
Cited by
23
References
3
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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Wang, Y., Liu, Z., Chen, Q., Yi, L., Xu, Z., Cai, M., Qin, J., Zhang, Y., Du, G., Hong, J., Guo, X., & Liu, C. (2022). Isolation and characterization of novel Fusobacterium nucleatum bacteriophages. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2022.945315