The Siderophore Phymabactin Facilitates the Growth of the Legume Symbiont Paraburkholderia phymatum in Aluminium-Rich Martian Soil

Abstract

Beneficial interactions between nitrogen-fixing soil bacteria and legumes offer a solution to increase crop yield on Earth and potentially in future Martian colonies. Paraburkholderia phymatum is a nitrogen-fixing beta-rhizobium, which enters symbiosis with more than 50 legumes and can survive in acidic or aluminium-rich soils. In a previous RNA-sequencing study, we showed that the beta-rhizobium P. phymatum grows well in simulated microgravity and identified phymabactin as the only siderophore produced by this strain. Here, the growth of the beta-rhizobium P. phymatum was assessed in Martian simulant soil using Enhanced Mojave Mars Simulant 2 (MMS-2), which contains a high amount of iron (18.4 percent by weight) and aluminium (13.1 percent by weight). While P. phymatum wild-type’s growth was not affected by exposure to MMS-2, a mutant strain impaired in siderophore biosynthesis (ΔphmJK) grew less than P. phymatum wild-type on gradient plates in the presence of a high concentration of MMS-2 or aluminium. This result suggests that the P. phymatum siderophore phymabactin alleviates aluminium-induced heavy metal stress. Ultra-high performance liquid chromatography–mass spectrometry (UHPLC-MS) showed that phymabactin can bind to aluminium more efficiently than iron. These results not only deepen our understanding of the behaviour of rhizobia in simulated extraterrestrial environments but also provide new insights into the potential use of P. phymatum for bioremediation of aluminium-rich soils and the multiple roles of the siderophore phymabactin.