Deep photoautotrophic prokaryotes contribute substantially to carbon dynamics in oxygen-deficient waters in a permanently redox-stratified freshwater lake

In lakes, seasonal phytoplankton blooms and allochthonous plant debris intensify particulate organic carbon fluxes to the lakebed. Microbes associated with these particles likely vary with organic substrate lability and redox conditions. To explore microbial compositional responses to these variables, we analyzed particle-associated and free-living assemblages in the permanently redox-stratified Fayetteville Green Lake using 16 S rRNA amplicon sequencing during the peak and end of cyanobacterial and photoautotrophic sulfur bacterial blooms. Assemblage compositions were strongly influenced by redox conditions and particle association. Assemblage compositions varied seasonally above the lower oxycline boundary (summer-generalist heterotrophs; autumn-iron reducers and specialist heterotrophs), but not in the anoxic region below. Particle-associated assemblages were less diverse than free-living assemblages and were dominated by heterotrophs that putatively metabolize complex organic substrates, purple sulfur bacteria, sulfur-cycling Desulfocapsa, and eukaryotic algae. The least diverse particle-associated assemblages occurred near the lower oxycline boundary, where microbial activities and abundances were highest, and anoxygenic photoautotrophs were enriched. The low-diversity particle-associated heterotrophs likely remineralize complex organic substrates, releasing simpler organic substrates to free-living assemblages during transit, thereby influencing surrounding microbial diversity and function. Our results challenge the paradigm that phytoplankton from the shallow photic zone are the primary contributor to the vertical flux. We suggest that photoautotrophic prokaryotes from the deep photic zone contribute significantly to deep-water carbon in this environment, and possibly in other oxygen-deficient waters with sulfidic photic zones. Furthermore, results suggest that seasonally variable terrestrial carbon and metal inputs also influence microbial diversity and function in similar systems.