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. 2022 Jul 15:13:903861.
doi: 10.3389/fmicb.2022.903861. eCollection 2022.

Analysis of intact prophages in genomes of Paenibacillus larvae: An important pathogen for bees

Henrique G Ribeiro  1   2 , Anna Nilsson  3 , Luís D R Melo  1   2 , Ana Oliveira  1   2
Affiliations

Analysis of intact prophages in genomes of Paenibacillus larvae: An important pathogen for bees

Henrique G Ribeiro et al. Front Microbiol. .

Abstract

Paenibacillus larvae is the etiological agent of American Foulbrood (AFB), a highly contagious and worldwide spread bacterial disease that affects honeybee brood. In this study, all complete P. larvae genomes available on the NCBI database were analyzed in order to detect presence of prophages using the PHASTER software. A total of 55 intact prophages were identified in 11 P. larvae genomes (5.0 ± 2.3 per genome) and were further investigated for the presence of genes encoding relevant traits related to P. larvae. A closer look at the prophage genomes revealed the presence of several putative genes such as metabolic and antimicrobial resistance genes, toxins or bacteriocins, potentially influencing host performance. Some of the coding DNA sequences (CDS) were present in all ERIC-genotypes, while others were only found in a specific genotype. While CDS encoding toxins and antitoxins such as HicB and MazE were found in prophages of all bacterial genotypes, others, from the same category, were provided by prophages particularly to ERIC I (enhancin-like toxin), ERIC II (antitoxin SocA) and ERIC V strains (subunit of Panton-Valentine leukocidin system (PVL) LukF-PV). This is the first in-depth analysis of P. larvae prophages. It provides better knowledge on their impact in the evolution of virulence and fitness of P. larvae, by discovering new features assigned by the viruses.

Keywords: Paenibacillus larvae; bacterial evolution; bacterial fitness; bacterial virulence; prophage.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Prophage prevalence in Paenibacillus larvae genomes: (A) Percentage of hosts with ≥ one and ≥ five intact prophages and ≥ one and ≥ eight defective prophages. (B) Whisker plots of prophage frequency per bacterial genome (total, defective and intact) before and after manual curing. Raw data provided directly from PHASTER, cured data results from manual verification. The horizontal line of each box represents the average prophages per genome and the external edges to the minimum/maximum number. (C) Average of total, defective, and intact prophages present per host genome. The error bars indicate the SD. Statistically significant, if value of p < 0.05 (*).
Figure 2
Figure 2
Number of prophages per size of host Paenibacillus larvae genomes: (A) total (B) intact (C) defective.
Figure 3
Figure 3
Average number of prophages (intact and defective) present per ERIC genotype (ERIC I-V). The error bars indicate the SD. Statistically significant, if value of p < 0.05 (*).
Figure 4
Figure 4
List of categories Cluster of Orthologous Groups (COG). Frequency (%) of prophage-derived CDS with a given function per COG.
Figure 5
Figure 5
Phylogenetic analysis of Paenibacillus larvae phages. Whole genomes based on shared CDS content (nucleotide), obtained with Geneious. Database: Paenibacillus larvae reported phages (n = 50) and intact Paenibacillus larvae prophages (n = 55), identified here. Clusters have ≥60% of shared CDS and were highlighted by colored rectangles.
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