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The genus “ Candidatus Kouleothrix” (Eikelboom type 1851) is the major filamentous bacterium responsible for activated sludge bulking in Japanese activated sludge plants, where it is present in many in unusually high abundances. Global surveys have shown this genus embraces several species, although the contribution each of these makes to bulking is not known. This study followed their population dynamics in a full-scale bulking sludge plant in Japan over a 12-month period, which required the development of species-specific FISH probes, used to measure their relative abundances. Six of the 9 recognised species of “ Ca . Kouleothrix” were detected there, two of which (midas_s_3423 and midas_s_35412) were at consistently high abundances and responsible for increases in the sludge volume index (SVI). Their abundances were also statistically correlated with their filament lengths, which showed higher correlations with SVI increases than did species abundances. This study examined the impacts of both operational parameters and other communities on the abundances of these two species over the 12-month period and showed marked interspecies differences in responses to both. Together these findings stress the importance in studies of this kind to identify populations to species level to reveal possible important ecological differences not seen at the genus level.