Marine bacteria cross-feeding controls the fate of extracellular glycolate carbon

Abstract

Glycolate is a major product of phytoplankton photorespiration, but its fate in the microbial food web is not well constrained. Here, we used stable isotope probing and mass spectrometry combined with genomic analyses and microscopy to quantify glycolate metabolism by a taxonomically diverse set of heterotrophic marine bacteria. We found that 9 of 16 tested strains with the genomic capability to metabolize glycolate directly assimilated and respired glycolate carbon in monoculture. We next co-cultivated glycolate-incorporating strains with non-incorporating strains and found that several cross-feeders incorporated more glycolate carbon into their biomass than direct incorporators. Carbon use efficiency, reflecting proportional differences in movement of glycolate carbon into biomass versus into carbon dioxide, were distinct across co-cultures and ranged from 0.01 -3.15% depending on the strain mixtures. These results suggest that the fate of glycolate carbon is not limited to microbial taxa with the genetic capability for direct assimilation, and that bacterial metabolic interactions via cross-feeding play a critical role in influencing the efficiency of carbon transfer. Such information is critical to refine conceptual and numerical models of heterotrophic processing and transfer of organic carbon in an era of global change with predicted increases in photorespiration.