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Distinct gene clusters drive formation of ferrosome organelles in bacteria

ABSTRACT: Cellular iron homeostasis is vital and maintained through tight regulation of iron import, efflux, storage and detoxification1-3. The most common modes of iron storage use proteinaceous compartments, such as ferritins and related proteins4,5. Although lipid-bounded iron compartments have also been described, the basis for their formation and function remains unknown6,7. Here we focus on one such compartment, herein named the 'ferrosome', that was previously observed in the anaerobic bacterium Desulfovibrio magneticus6. Using a proteomic approach, we identify three ferrosome-associated (Fez) proteins that are responsible for forming ferrosomes in D. magneticus. Fez proteins are encoded in a putative operon and include FezB, a P1B-6-ATPase found in phylogenetically and metabolically diverse species of bacteria and archaea. We show that two other bacterial species, Rhodopseudomonas palustris and Shewanella putrefaciens, make ferrosomes through the action of their six-gene fez operon. Additionally, we find that fez operons are sufficient for ferrosome formation in foreign hosts. Using S. putrefaciens as a model, we show that ferrosomes probably have a role in the anaerobic adaptation to iron starvation. Overall, this work establishes ferrosomes as a new class of iron storage organelles and sets the stage for studying their formation and structure in diverse microorganisms.

INSTRUMENT(S): Synapt G2-S HDMS

ORGANISM(S): Desulfovibrio Magneticus Rs-1 Bacteria

SUBMITTER: Carly Grant

LAB HEAD: Arash Komeili

PROVIDER: PXD017470 | Pride | 2022-05-31

REPOSITORIES: Pride

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Distinct gene clusters drive formation of ferrosome organelles in bacteria.

Grant Carly R CR Amor Matthieu M Trujillo Hector A HA Krishnapura Sunaya S Iavarone Anthony T AT Komeili Arash A

Nature 20220518 7912

Cellular iron homeostasis is vital and maintained through tight regulation of iron import, efflux, storage and detoxification1-3. The most common modes of iron storage use proteinaceous compartments, such as ferritins and related proteins4,5. Although lipid-bounded iron compartments have also been described, the basis for their formation and function remains unknown6,7. Here we focus on one such compartment, herein named the 'ferrosome', that was previously obser ...[more]

PMID: 35585231

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Project description:This a model from the article: Systems analysis of iron metabolism: the network of iron pools and fluxes Tiago JS Lopes, Tatyana Luganskaja, Maja Vujic-Spasic, Matthias W Hentze, Martina U Muckenthaler, Klaus Schumann and Jens G Reich BMC Systems Biology2010, Aug 13;4(1):112. 20704761, Abstract: Background Every cell of the mammalian organism needs iron in numerous oxido-reductive processes as well as for transport and storage of oxygen. The versatility of ionic iron makes it a toxic entity which can catalyze the production of radicals that damage vital membranous and macromolecular assemblies in the cell. The mammalian organism maintains therefore a complex regulatory network of iron uptake, excretion and intra-body distribution. Intracellular regulation in different cell types is intertwined with a global hormonal signaling structure. Iron deficiency as well as excess of iron are frequent and serious human disorders. They can affect every cell, but also the organism as a whole. Results Here, we present a kinematic model of the dynamic system of iron pools and fluxes. It is based on ferrokinetic data and chemical measurements in C57BL6 wild-type mice maintained on iron-deficient, iron-adequate, or iron-loaded diet. The tracer iron levels in major tissues and organs (16 compartment) were followed for 28 days. The evaluation resulted in a whole-body model of fractional clearance rates. The analysis permits calculation of absolute flux rates in the steady-state, of iron distribution into different organs, of tracer-accessible pool sizes and of residence times of iron in the different compartments in response to three states of iron-repletion induced by the dietary regime. Conclusions This mathematical model presents a comprehensive physiological picture of mice under three different diets with varying iron contents. The quantitative results reflect systemic properties of iron metabolism: dynamic closedness, hierarchy of time scales, switch-over response and dynamics of iron storage in parenchymal organs. Therefore, we could assess which parameters will change under dietary perturbations and study in quantitative terms when those changes take place. This model corresponds to the Iron Loaded condition - Mice This model originates from BioModels Database: A Database of Annotated Published Models. It is copyright (c) 2005-2010 The BioModels Team.For more information see the terms of use.To cite BioModels Database, please use Le Novère N., Bornstein B., Broicher A., Courtot M., Donizelli M., Dharuri H., Li L., Sauro H., Schilstra M., Shapiro B., Snoep J.L., Hucka M. (2006) BioModels Database: A Free, Centralized Database of Curated, Published, Quantitative Kinetic Models of Biochemical and Cellular Systems Nucleic Acids Res., 34: D689-D691.

Project description:Recently described microarray studies have defined the genes that are regulated in response to iron and heme levels in three isolates of Haemophilus influenzae. Comparison of the data sets have allowed us to develop a putative core iron/heme modulon. Included in the core modulon are thirty seven genes that are preferentially expressed under iron/heme limitation. The majority of these genes are involved with iron and or heme acquisition such as hitA, tonB, exbD, exbB, hgpB, hgpC and the hxu and tbp operons. In addition, we identified several other loci with roles potentially related to iron and heme metabolism such as protection against oxidative stress, iron and heme storage and detoxification and biofilm formation. In this report, we describe the further definition of the core iron/heme modulon following transcriptomic analysis of H. influenzae strains 86028NP and R2846. With the defined core, we then test our original hypothesis that M-bM-^@M-^\iron and heme regulated genes are upregulated, and important, during clinical infectionM-bM-^@M-^]. The in vivo expression profiles of the core genes were determined following inoculation of select isolates into the bullae of chinchillas. Isolates selected included 86028NP and a previously un-characterized isolate HI1722. To facilitate studies with the latter isolate, we sequenced the genome and annotated the identified CDS to ensure that oligonucleotides selected for Q-PCR would correctly target each gene of interest. The results from the in vitro studies show that the operons identified as core are actively upregulated in the chinchilla ear during otitis media. For isolate 86-028NP, 70% of the operons were significantly upregulated while isolate NTHI1722 had 100% of the operons upregulated. Three replicate cultures were grown in iron and heme depleted media for 90 minutes and samples taken for expression analyses. Fe and heme were supplemented to the remaining cultures and the cultures allowed to incubate an additional 20 minutes. Microarray analyses were used to determine changes in gene expression resulting from transfer from FeHm-deplete to FeHm-replete conditions.

			Action	DRS
	Results.zip	Other
	ferrosomes_r1.raw.zip	Raw
	ferrosomes_r2.raw.zip	Raw
	ferrosomes_r3.raw.zip	Raw
	lysate_r1.raw.zip	Raw