The Role of the Glyoxylate Shunt in the Acclimation to Iron Limitation in Marine Heterotrophic Bacteria

Iron (Fe) is an essential element for marine microbial growth but is present in trace amounts (<0.1 nM) in surface waters of the ocean. In heterotrophic bacteria, Felimitation particularly impacts ATP production as Fe is an essential co-factor of enzymes involved in the electron-transport chain as well as the tricarboxylic acid (TCA) cycle. Fe-limitation can therefore drastically reduce both bacterial growth and respiration, consequently affecting the efficiency of organic carbon remineralization. Heterotrophic bacteria possess various strategies to cope with Fe-limitation. In the present study we tested the hypothesis that the induction of the glyoxylate shunt can represent one such strategy. Genetic approaches were used to gain insight into the potential role the glyoxylate shunt may have in alleviating Fe-stress using the gammaproteobacterium, Photobacterium angustum S14. A recombinant bioluminescent reporter of P angustum S14 (icl-luc) revealed a strong and significant increase in the expression of isocitrate lyase (icl), a key enzyme within the glyoxylate shunt, when cells were subjected to strong Fe-limitation. Although the growth and respiration rates decreased for both the wildtype and an id knockout mutant (Delta icl) under strong Fe-limitation, they were +/- 30% lower for Delta icl as compared to the wildtype. Complementation of Delta icl restored the growth and respiration rates to those observed in the wildtype, further confirming the importance of the glyoxylate shunt under strong Fe-limitation. Due to the ubiquitous nature of the glyoxylate shunt within marine bacteria, our results lead us to propose this pathway as an important acclimation strategy for marine heterotrophic bacteria that are subjected to Fe-limitation.