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Glaciers harbour diverse microbes and autotrophic microbes play a key role in sustaining the glacial ecosystems by providing organic carbon. The succession of glacier-originated autotrophic microbes and their effects on downstream aquatic ecosystems remain unknown. We herein investigated the shift of autotrophic microbial communities in waters (not biofilms) along a glacier meltwater transect consisting of a glacier terminus outflow (subglacial), a glacial stream, two glacier-fed lakes (upper and lower) and their outflow on the Tibetan Plateau. The autotrophic community was characterized by cbbL gene using qPCR, T-RFLP and clone library/sequencing methods. The results demonstrated that form IC and ID autotrophic microbes exhibited a much higher abundance than form IAB in all waters along the transect. Form IAB autotrophic abundance in waters gradually decreased, while the form IC exhibited a substantial increase in the upper lake waters, and ID exhibited a substantial increase in the lower lake waters. The water form IC autotrophic community structure exhibited a distinguished shift from the glacier terminus outflow to the stream, while the form ID showed a dramatic shift from the stream to the lower lake. Our results revealed the succession patterns of glacier-originated autotrophic microbial communities and possible effects on downstream aquatic ecosystems.