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. 2007 Nov;73(21):6730-9.
doi: 10.1128/AEM.01399-07. Epub 2007 Aug 31.

Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts

Karin Holmfeldt  1 , Mathias Middelboe, Ole Nybroe, Lasse Riemann
Affiliations

Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts

Karin Holmfeldt et al. Appl Environ Microbiol. 2007 Nov.

Abstract

Phages are a main mortality factor for marine bacterioplankton and are thought to regulate bacterial community composition through host-specific infection and lysis. In the present study we demonstrate for a marine phage-host assemblage that interactions are complex and that specificity and efficiency of infection and lysis are highly variable among phages infectious to strains of the same bacterial species. Twenty-three Bacteroidetes strains and 46 phages from Swedish and Danish coastal waters were analyzed. Based on genotypic and phenotypic analyses, 21 of the isolates could be considered strains of Cellulophaga baltica (Flavobacteriaceae). Nevertheless, all bacterial strains showed unique phage susceptibility patterns and differed by up to 6 orders of magnitude in sensitivity to the same titer of phage. The isolated phages showed pronounced variations in genome size (8 to >242 kb) and host range (infecting 1 to 20 bacterial strains). Our data indicate that marine bacterioplankton are susceptible to multiple co-occurring phages and that sensitivity towards phage infection is strain specific and exists as a continuum between highly sensitive and resistant, implying an extremely complex web of phage-host interactions. Hence, effects of phages on bacterioplankton community composition and dynamics may go undetected in studies where strain identity is not resolvable, i.e., in studies based on the phylogenetic resolution provided by 16S rRNA gene or internal transcribed spacer sequences.

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Figures

FIG. 1.
FIG. 1.
Sampling sites for bacterial (b) and phage (p) isolations. Exact locations are marked by arrows. b1, Hirsholm; b2, Ellekilde Hage; b3, Svaneke; b4, Øresund; b5, off Öland. The map was generated using the Online Map Creation software (http://www.aquarius.geomar.de/omc/).
FIG. 2.
FIG. 2.
Neighbor-joining trees showing the phylogenetic relationships between bacteria used in this study. Trees are based on 16S rRNA gene sequences (∼800 bp) (A) and ITS gene sequences (∼675 bp) (B). Phylogenetic relationships were bootstrapped 1,000 times, and values greater than 50% are shown.
FIG. 3.
FIG. 3.
Genomic profiling of bacterial isolates. An agarose gel showing UP-PCR banding patterns for 15 of the 23 bacterial isolates analyzed is shown. Identical strains (e.g., strains NN015839 and NN015840) and strains with differences (e.g., strains 10 and 12) are displayed.
FIG. 4.
FIG. 4.
Genomic characterization of phages. (A) PFGE analysis of genomic DNAs from 9 of the 46 phage isolates used in this study. The gel displays phages with identical (e.g., φ12:4 and φ12:5) and different (e.g., φ18:3 and φ39:1) genomes sizes. (B) HindIII restriction digests of eight phage genomes. Cleavage patterns for phages with identical (φ12:4 and φ12:5) and different (e.g., φ17:1 and φ18:1) infectivity patterns are shown along with patterns for phages with almost identical infectivity patterns (φ4:1 and φ17:2; see Fig. 6). Arrowheads indicate differences in banding patterns for φ4:1 and φ17:2. See Table 2 for phage genome sizes.
FIG. 5.
FIG. 5.
TEM of selected C. baltica phages. Bars, 50 nm. (A) φ40:2; (B) φ18:4; (C) φ18:4; (D) φ38:1; (E) φ13:1; (F) φ39:1; (G) φ4:1; (H) φ3:2; (I) φ18:1; (J) φ12:1; (K) φSM; (L) φ10:1. The phage φ18:4 lysate included two morphotypes (B and C). Examples of phages with identical genome sizes but with different morphotypes are shown (e.g., I versus J and K versus L). Genome sizes and host ranges for the phages shown are given in Table 2 and Fig. 6.
FIG. 6.
FIG. 6.
Host ranges of the 46 phages. Gray squares indicate lysis and white squares indicate no lysis.
FIG. 7.
FIG. 7.
UPGMA tree based on susceptibility to phages infection. The data shown in Fig. 6 were scored and converted to pairwise distances using the Dice similarity coefficient. Groupings of bacterial strains according to UP-PCR and LPS profiling and colony morphology are inserted to facilitate comparison.
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