Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix

Abstract

Populations of the cyanobacterium Planktothrix comprise multiple coexisting oligopeptide chemotypes that can behave differently in nature. We tested whether this population subdivision can, in principle, be driven by parasitic chytrid fungi, which are almost neglected agents of Planktothrix mortality. Two chytrid strains, Chy-Lys2009 and Chy-Kol2008, were isolated from Planktothrix-dominated lakes in Norway. The two strains shared 98.2% and 86.2% of their 28S and internal transcribe spacer rRNA gene sequences, respectively. A phylogenetic analysis placed them in the order Rhizophydiales family Angulomycetaceae. Chy-Lys2009 and Chy-Kol2008 could completely lyse Planktothrix cultures within days, while they failed to infect other filamentous cyanobacteria. The effect on Planktothrix was chemotype dependent, and both chytrid strains showed distinct chemotype preferences. These findings identify chytrid fungi infecting Planktothrix as highly potent and specialized parasites which may exert strong selective pressure on their hosts. According to established hypotheses on host-parasite coevolution, parasitism with the above properties may result in subdivision of Planktothrix populations into coexisting chemotypes and periodic shifts in the relative Planktothrix chemotype composition. These predictions are in agreement with field observations. Moreover, a genetic analysis verified the co-occurrence of Chy-Lys2009 and Chy-Kol2008 or related chytrid strains along with distinct Planktothrix chemotypes in at least one water body. Our findings are consistent with a scenario where chytrid parasitism is one driving force of Planktothrix population subdivision, which in turn leads to polymorphism in parasitic chytrid fungi. Future studies should test the validity of this scenario under field conditions.

FIG. 1.

Properties of Planktothrix sp. strains that were used in this study. Shown for each strain are its chemotype affiliation, its identification number in the NIVA culture collection, when and from which water body it was isolated, if it contained the pigment phycoerythrin, and its cellular oligopeptide composition. For each oligopeptide, the name and its molecular mass (in daltons, in parentheses) are given. The oligopeptides are sorted by structural class. Mcyst, microcystin. Strains with phycoerythrin correspond to P. rubescens, and those without the pigment correspond to P. agardhii. Lakes Långsjön and Vesijärvi are situated in Finland. All other lakes are situated in southeastern Norway. All data are taken from Rohrlack and coworkers (36).

FIG. 2.

Infection intensity in Planktothrix sp. strains representing chemotypes Cht1, Cht5, Cht7a to Cht7e, and Cht9 exposed to chytrid strains Chy-Lys2009 and Chy-Kol2008 for 7 days. Intensity was measured according to the following scale: 0, no sporangia, no active zoospores, 1, up to 10% of host filaments with sporangia, active zoospores present; 2, 10 to 50% of host filaments with sporangia, active zoospores present; 3, 50 to 90% of host filaments with sporangia, active zoospores present; 4, 90 to 100% of host filaments with sporangia, active zoospores present; 5, final stage of infection, most host filaments disintegrated, numerous sporangia visible, and active zoospores present or absent. Each column represents the mean value of tree replicates with the respective standard deviation.