Disentangling the relative influence of bacterioplankton phylogeny and metabolism on lysogeny in reservoirs and lagoons

Abstract

Previous studies indicate that lysogeny is preponderant when environmental conditions are challenging for the bacterial communities and when their metabolism is reduced. Furthermore, it appears that lysogeny is more frequent within certain bacterial phylogenetic groups. In this comparative study from 10 freshwater reservoirs and 10 coastal lagoons, we aim to disentangle the influence of these different factors. In eight reservoirs and four lagoons, lysogeny was detected by induction assays with mitomycin C, and induction significantly modified the bacterial community composition (BCC), whereas community composition remained constant in ecosystems in which lysogeny was not observed. Among the phylogenetic groups studied, the most abundant ones were Bacteroidetes and α-proteobacteria in lagoons, and β-proteobacteria and Bacteroidetes in reservoirs. These dominant groups comprised the highest proportions of inducible lysogens. In order to unravel the effects of bacterial metabolism from phylogeny on lysogeny, we measured bacterial community physiology and the specific activities of selected phylogenetic groups. The proportion of inducible lysogens within the α- and the β-proteobacteria decreased with increasing group-specific metabolism in lagoons and reservoirs, respectively. In contrast, this relationship was not observed for the other lysogen-containing groups. Hence, both host physiology and phylogeny are critical for the establishment of lysogeny. This study illustrates the importance of lysogeny among the most abundant phylogenetic groups, and further suggests its strong structuring impact on BCC.

Figure 1

Linear correlations between the frequency of lysogenic cells calculated from minimum (black circle, FLC_minBS) and maximum (open circle, FLC_maxBS) burst size and (a) the proportion of Bacteria (% EUB) in coastal lagoons, and (b) the proportion of respiring bacterial cells (% CTC⁺) in reservoirs.

Figure 2

Box plots of the Δ_P of each bacterial phylogenetic group (see Materials and methods for Δ_P calculation) in (a) ecosystems without detected induction, (b) coastal lagoons with induction and (c) freshwater reservoirs with induction. Each box comprises the two middle quartiles, separated by the median. The whiskers represent 1.5 times the inner quartile spread in length, and provide an arbitrary cut-off point to identify data points that possibly are outside values. The small circles denote outlier values.

Figure 3

: Example of bacterial community composition changes in a system without induction (a, b), Campignol lagoon and with induction (c, d, Fréjorgues reservoir). (a, c) Are control samples, and (b, d) are mitomycin C-amended incubations. Data are expressed as percentages of total DAPI counts. Error bars were determined from a subset of replicated samples (see Materials and methods).

Figure 4

Linear correlations between the proportions of leucine-assimilating bacterial cells and the Δ_P values within three different bacterial phylogenetic groups. Left panel: coastal lagoons. Right panel: freshwater reservoirs.