Temporal dynamics of microbial metabolic processes under hyporheic fluctuation

Abstract:

River corridors are highly dynamic systems that are major players in the earth’s biogeochemical cycles; yet, temporal resolution into the microbial engines of biogeochemical cycles in these systems is severely lacking. Here, we investigate the temporal dynamics of a groundwater-surface water mixing (hyporheic) zone using ultrahigh resolution metabolomics, transcriptomics, and oxygen consumption measurements using a monthlong timeseries to couple the mechanisms of biogeochemical change to aerobic respiration. We find that metabolomic changes coincide with changes in surface water elevation and generally induce a lagged response in aerobic respiration of one day or more. Additionally, we unravel core metabolomic transformations central to the maintenance of function under hyporheic fluctuations as well as an auxiliary set of metabolomic processes that are dominant under high- vs. low- periods of aerobic respiration. We also use multi ‘omic networks to associate active microorganisms, and specific active metabolic processes in sediment microbiomes, with modules of metabolomic transformations. Our results highlight a disconnect between the scales of molecular mechanisms that are increasingly represented in microbial-explicit models and the ecosystem-level responses they invoke. We also use multiple data streams to provide unprecedented resolution into the molecular drivers of biogeochemistry in hyporheic zones. Taken together, we propose that asynchronous processes at the molecular-to-ecosystem can lead to spurious model predictions, and we reveal important molecular processes for deeper investigation within river corridors.

River corridors are highly dynamic systems that are major players in the earth’s biogeochemical cycles; yet, temporal resolution into the microbial engines of biogeochemical cycles in these systems is severely lacking. Here, we investigate the temporal dynamics of a groundwater-surface water mixing (hyporheic) zone using ultrahigh resolution metabolomics, transcriptomics, and oxygen consumption measurements using a monthlong timeseries to couple the mechanisms of biogeochemical change to aerobic respiration. We find that metabolomic changes coincide with changes in surface water elevation and generally induce a lagged response in aerobic respiration of one day or more. Additionally, we unravel core metabolomic transformations central to the maintenance of function under hyporheic fluctuations as well as an auxiliary set of metabolomic processes that are dominant under high- vs. low- periods of aerobic respiration. We also use multi ‘omic networks to associate active microorganisms, and specific active metabolic processes in sediment microbiomes, with modules of metabolomic transformations. Our results highlight a disconnect between the scales of molecular mechanisms that are increasingly represented in microbial-explicit models and the ecosystem-level responses they invoke. We also use multiple data streams to provide unprecedented resolution into the molecular drivers of biogeochemistry in hyporheic zones. Taken together, we propose that asynchronous processes at the molecular-to-ecosystem scale can lead to spurious model predictions, and we reveal important molecular processes for deeper investigation within river corridors.