Light-dark fluctuated metabolic features of diazotrophic and non-diazotrophic cyanobacteria and their coexisting bacteria

Abstract

Cyanobacteria, the most abundant photosynthetic organisms in oceans, are tightly associated with diverse microbiota. However, the relationships between heterotrophic bacteria and cyanobacteria, particularly the diazotrophic group, are not fully understood. Here, we compared diel gene expressions of N2 fixing cyanobacteria Crocosphaera watsonii WH0003 and non-diazotrophic Synechococcus sp. RS9902 and their associated bacteria using metatranscriptomics approach. WH0003 showed significant up-regulation of O2 restriction and oxidative phosphorylation related genes at nighttime due to large carbon and energy investments for active N2 fixation. In contrast, RS9902 had higher expression for those genes at daytime. The two cyanobacteria hosted distinct bacterial communities with clear separate substrate utilization niches to reduce competition. Light-dark partitioning of nutrient acquisition among the dominant bacterial groups likely contributed to the dynamic balance for community coexistence. Moreover, particle-attached (PA) bacteria in RS9902 largely expressed glycoside hydrolases to hydrolyze complex carbohydrate compounds, while free-living (FL) bacteria priorly assimilated soluble, diffusible molecules. Spatial partitioning of nutrient acquisition between PA and FL bacteria implied that location initially influenced metabolic features of host associated bacteria. Our results advance knowledge on light-dark regulated metabolic activities of diazotrophic and non-diazotrophic cyanobacteria, and provide new insights into the coexisting strategies of different bacterial groups.