Syntrophic splitting of central carbon metabolism in host cells bearing functionally different symbiotic bacteria

Abstract

Insects feeding on the nutrient-poor diet of xylem plant sap generally bear two microbial symbionts that are localized to different organs (bacteriomes) and provide complementary sets of essential amino acids (EAAs). Here, we investigate the metabolic basis for the apparent paradox that xylem-feeding insects are under intense selection for metabolic efficiency but incur the cost of maintaining two symbionts for functions mediated by one symbiont in other associations. Using stable isotope analysis of central carbon metabolism and metabolic modeling, we provide evidence that the bacteriomes of the spittlebug Clastoptera proteus display high rates of aerobic glycolysis, with syntrophic splitting of glucose oxidation. Specifically, our data suggest that one bacteriome (containing the bacterium Sulcia, which synthesizes seven EAAs) predominantly processes glucose glycolytically, producing pyruvate and lactate, and the exported pyruvate and lactate is assimilated by the second bacteriome (containing the bacterium Zinderia, which synthesizes three energetically costly EAAs) and channeled through the TCA cycle for energy generation by oxidative phosphorylation. We, furthermore, calculate that this metabolic arrangement supports the high ATP demand in Zinderia bacteriomes for Zinderia-mediated synthesis of energy-intensive EAAs. We predict that metabolite cross-feeding among host cells may be widespread in animal–microbe symbioses utilizing low-nutrient diets.

Bacterial symbiont subpopulations have different roles in a deep-sea symbiosis

“…At the same time, the respective disadvantages are avoided (large Endoriftia would need to invest much more resources in cell division and replication of their multiple genome copies than small cells, while smaller Endoriftia could not produce as much biomass as large symbionts). Increased metabolic efficiency as a consequence of specialized bacteria performing complementary tasks has also been reported for different bacterial species and strains working together in other symbioses ( Zheng et al, 2019 ; Ankrah et al, 2020 ). In Riftia , the largest symbionts that are digested at the trophosome lobule periphery are those with the highest nutritional value.…”

The Evolution of Interdependence in a Four-Way Mealybug Symbiosis

“…Although the genomes of the gammaproteobacterial symbionts of P. longispinus are still large, the pseudogenization of nearly half of their genes allows us to ask whether gene inactivation events show nascent signals of the interdependency that is common in more established endosymbionts ( Martin and Herrmann 1998 ; Shigenobu 200l; Wu et al 2006 ; Gosalbes et al 2008 ; McCutcheon and Moran 2010 ; Lamelas et al 2011 ; Sloan and Moran 2012 ; Husník et al 2013 ; López-Madrigal et al 2013 ; Bennett et al 2014 ; Santos-Garcia et al 2014 ; Luan et al 2015 ; Husník and McCutcheon 2016 ; Szabó et al 2017 ; Ankrah et al 2020 ). Clear patterns of complementary gene loss and retention have been observed in other mealybug symbioses that host intra- Tremblaya gammaproteobacterial symbionts, but in these other cases, the gammaproteobacterial endosymbionts have highly reduced and gene-dense genomes of less than 1 Mb, consistent with much longer periods of host restriction ( Husník and McCutcheon 2016 ; Szabó et al 2017 ).…”

The Symbiotic “All-Rounders”: Partnerships between Marine Animals and Chemosynthetic Nitrogen-Fixing Bacteria

“…If genetically homogenous but physiologically distinct symbiont subpopulations inhabit different regions of the gill or bacteriocytes, they may have different functions in the symbiosis; it is conceivable that the “labor” of symbiosis is divided into a subpopulation that provides carbon and another one that provides nitrogen. Having distinct cells “tuned” to a particular metabolic task can enhance the efficiency of a genetically homogenous population ( 86 ). Partitioning of nitrogen and carbon fixation into distinct cells is seen in some multicellular cyanobacteria, although restricting nitrogen fixation to dedicated heterocyst cells is primarily thought to protect nitrogenase from the oxygen produced through photosynthesis, rather than the ambient environment as we propose in the lucinid symbionts ( 87 ).…”