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

Abstract

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.In permanently redox-stratified water bodies, biogenic particles sink through redox zones, and each zone has distinctive free-living planktonic microbial assemblages (Fuchsman et al. 2011;Suter et al. 2018). The interplay between particle-associated microbes and those free-living in surrounding waters likely differs among redox zones. Redox conditions can vary at macroscales with lake depth and at microscales within particles themselves (Wright et al. 2012).

Preserved particulate organic carbon is likely derived from the subsurface sulfidic photic zone of the Proterozoic Ocean: evidence from a modern, oxygen‐deficient lake

“…Our qPCR (Figure 7), microscopy (Figure S2), and field data (Figures 1, 2) agree with our 2017 amplicon libraries, showing that the light-scattering layer consisted of three distinctive photoautotrophic populations that are physically partitioned by their light requirements and hydrogen sulfide tolerances (Cohen et al, 2023).…”

“…Because cells that aggregate or associate with particles are more commonly buried in sediments owing to their faster settling velocities relative to small suspended individual cells (Alldredge & Gotschalk, 1988), we analyzed size-fractionated particulate matter. We compare current results with size-fractionated autotrophic and methane-cycling phylotype distributions previously determined by 16S rRNA amplicon sequencing (Cohen et al, 2023). To provide a biogeochemical context, we profiled hydrographic and chemical features and microbial production rates.…”

“…Size-fractionated cbbL, cbbM, aclB, and mcrA functional gene depth profiles reflected distributions of cyanobacterial, purple sulfur and green sulfur bacterial photoautotrophic populations, and the methanogen Methanoregula, respectively, determined from amplicon libraries prepared from the same samples (Cohen et al, 2023;…”

“…For this study, the deepest part of the FGL water column (43°03′01.9"N, 75°57′58.9"W) was sampled on 28 July-4 August Because total inorganic carbon assimilation and bacterial heterotrophic production rates were profiled throughout the lake the previous summer (Cohen et al, 2023), we focused on profiling inor- rates were performed as previously described (Taylor et al, 2001, Cohen et al, 2023.…”

“…This analysis returns the best approximation of the biomass δ 13 C POC for each mass fraction (in our case, carbon fixation pathway). We also used the Cohen et al (2023) 16S rRNA library to calculate the expected δ 13 C POC value ranges to compare our measured values.…”