Petrobactin, a siderophore produced by Alteromonas, mediates community iron acquisition in the global ocean

Abstract

It is now widely accepted that siderophores play a role in marine iron biogeochemical cycling. However, the mechanisms by which siderophores affect the availability of iron from specific sources and the resulting significance of these processes on iron biogeochemical cycling as a whole have remained largely untested. In this study, we develop a model system for testing the effects of siderophore production on iron bioavailability using the marine copiotroph Alteromonas macleodii ATCC 27126. Through the generation of the knockout cell line ΔasbB::kmr, which lacks siderophore biosynthetic capabilities, we demonstrate that the production of the siderophore petrobactin enables the acquisition of iron from mineral sources and weaker iron-ligand complexes. Notably, the utilization of lithogenic iron, such as that from atmospheric dust, indicates a significant role for siderophores in the incorporation of new iron into marine systems. We have also detected petrobactin, a photoreactive siderophore, directly from seawater in the mid-latitudes of the North Pacific and have identified the biosynthetic pathway for petrobactin in bacterial metagenome-assembled genomes widely distributed across the global ocean. Together, these results improve our mechanistic understanding of the role of siderophore production in iron biogeochemical cycling in the marine environment wherein iron speciation, bioavailability, and residence time can be directly influenced by microbial activities.

Competitive Interactions Between Microbial Siderophores and Humic-Like Binding Sites in European Shelf Sea Waters

“…However, FeSid did not become the dominant species until the total siderophore concentration was 50% of the total dissolved iron concentration, and even when the total siderophore concentration is equal to the total dissolved iron concentration then approximately 25% of DFe was calculated as bound to the humic substance-like binding sites in DOM. These calculations are thus consistent with the apparent undersaturation of siderophores isolated from seawater observed in other studies (Boiteau et al, 2016;Manck et al, 2021).…”

“…We also note that marinobactins are mixed a-hydroxy carboxylate siderophores and, when complexed to iron, have greater sensitivity to photochemical degradation than hydroxamate type siderophores (Barbeau et al, 2003). Thus, it was notable that N 9 siderophores were most abundant below the photic zone, as recently observed for petrobactins, another photosenstive type of siderophore (Manck et al, 2021). We suggest that the bacterial species responsible for N 9 production may be more abundant in sub photic zone environments, where photochemical breakdown of siderophores would not occur.…”

“…Siderophores are secondary metabolites produced by bacteria and fungi in order to acquire iron (Hider and Kong, 2010) and are thought to make up a component of the dissolved iron pool in seawater, likely influencing iron bioavailability to marine microbes (Shaked and Lis, 2012;Hogle et al, 2021). More than forty siderophores from marine bacteria have been characterised (Vraspir and Butler, 2009) and four groups of these siderophores, ferrioxamines, amphibactins, synechobactins and petrobactins have been shown to occur in open ocean surface waters (Mawji et al, 2008;Boiteau et al, 2016;Velasquez et al, 2016;Bundy et al, 2018;Manck et al, 2021). The concentrations of individual siderophores have been determined to be of the order of a few picomoles per litre (Mawji et al, 2008;Bundy et al, 2018;Boiteau et al, 2019), similar in magnitude to other microbial exatometabolites (i.e.…”

Community Interaction Co-limitation: Nutrient Limitation in a Marine Microbial Community Context

“…Phytoplankton might benefit from accessing these inorganic nutrients, rather than producing the enzymes required for the conversion themselves. Additionally, production of siderophores by select community members could lead to an increase in ‘new’ bioavailable iron by mobilizing particulate iron ( Manck et al, 2022 ). The nutrient limiting the growth of siderophore producers could then possibly limit bioavailable iron delivery to the whole community, contributing to CIC.…”

Bacillus suaedae sp. nov., isolated from the stem of Suaeda aralocaspica in north-west China

“…The most similar known clusters with terpene, lassopeptide, ectoine, T3PKS and siderophore regions were carotenoid, paeninodin, ectoine, 7-deoxypactamycin and petrobactin, respectively. This indicates that strain YZJH907-2 T may produce these secondary metabolites, such as carotenoid, paeninodin, ectoine, 7-deoxypatamycin and petrobactin, which have the ability to promote plant growth and protect plants from biological and abiotic stresses [53, 58–62]. The other regions had such lower similarity compared to known clusters that the secondary metabolites could not be identified.…”