Phycosome dynamics during successive outdoor microalgae cultivation from late summer to fall

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Phycosomes, or algal microbiomes, can impact algal productivity, and the influence of phycosome succession and turnover may be magnified during stresses such as low temperature, low solar irradiance, and/or high pH. The combined effects of abiotic (e.g., temperature, irradiance) and ecological factors on biomass productivity in outdoor, open raceway cultivation were assessed on Chlorella SLA-04 in summer and fall conditions. Raceway ponds (200L) were used to grow outdoor SLA-04 cultures under high pH conditions (i.e., pH 8 to pH 12) in five sequential runs. SLA-04 cultures had the highest biomass productivity in early runs (R1, R2, and R3) when maximum and minimum temperatures as well as radiative flux were higher while both total dry weight and lipid levels declined with declining temperatures and light (R4 and R5). Despite lower overall biomass, chlorophyll did not decline to the same extent, and nitrate was still depleted albeit at a slower rate. The overall diversity of microbial communities (both bulk phase and algal associated) increased during the successive runs, and predominant bacterial groups shifted as temperature and light declined (R3). During R1 and R2, specific amplicon sequencing variants (ASVs) predominated (related to Paracoccus, Brevundimonas, Rhodococcus, and Rhizobium) and these ASVs declined in R3 as the light and temperature declined. These results are corroborated by decreased growth of a Paracoccus isolate at lower temperatures compared to SLA-04. As microbial growth slowed in R4 and R5, the following bacterial ASVs increased: Roseivivax, Porphyrobacter, unclassified GpV, Gemmata, Rhizobacter, and Luteolibacter. Overall, the results demonstrated that SLA-04 could tolerate transitions to lower temperatures (and light) compared to the present bacterial populations during outdoor cultivations, but total biomass productivity (ash free dry weight) and lipids (Nile Red fluorescence) decreased significantly. Coinciding with these changes, Flavobacteria and Deinococci ASVs that were associated with higher algal biomass and higher temperatures declined and different ASVs (Planctomycetes, Clostridia, Gemmatimonadetes, Chlamydia) were enriched during lower algal productivity and lower temperatures. Changes in the microbial community could be directly related to observed temperature shifts as well as indirectly related to SLA-04 growth dynamics during the temperature and/or light shifts. Weather (i.e., light and temperature) is predicted to have major impacts on large-scale algal production (Kleiman et al., 2021), and the presented results provide insight into the relationships between declining light/temperature, algal growth, and phycosome composition during successive, outdoor cultivations.