Iron metabolic pathways in the processes of sponge plasticity

Abstract

The ability to regulate oxygen consumption evolved in ancestral animals and is intrinsically linked to iron metabolism. The iron pathways have been intensively studied in mammals, whereas data on distant invertebrates are limited. Sea sponges represent the oldest animal phylum and have unique structural plasticity and capacity to reaggregate after complete dissociation. We studied iron metabolic factors and their expression during reaggregation in the White Sea cold-water sponges Halichondria panicea and Halisarca dujardini. De novo transcriptomes were assembled using RNA-Seq data, and evolutionary trends were analyzed with bioinformatic tools. Differential expression during reaggregation was studied for H. dujardini. Enzymes of the heme biosynthesis pathway and transport globins, neuroglobin (NGB) and androglobin (ADGB), were identified in sponges. The globins mutate at higher evolutionary rates than the heme synthesis enzymes. Highly conserved iron-regulatory protein 1 (IRP1) presumably interacts with the iron-responsive elements (IREs) found in mRNAs of ferritin (FTH1) and a putative transferrin receptor NAALAD2. The reaggregation process is accompanied by increased expression of IRP1, the antiapoptotic factor BCL2, the inflammation factor NFκB (p65), FTH1 and NGB, as well as by an increase in mitochondrial density. Our data indicate a complex mechanism of iron regulation in sponge structural plasticity and help to better understand general mechanisms of morphogenetic processes in multicellular species.

Conservative and Atypical Ferritins of Sponges

“…HRE motifs found in upstream regions of HdF1a and HdF2 (i.a. within CpG islands) presumably make them sensitive to hypoxia [15]; in turn, we have previously shown that hypoxic response is important for sponge reaggregation process [24]. HdF1a, HdF1b, and H. panicea's HpF1, like most Demospongiae and noninsect invertebrate ferritins, have mRNA hairpin motifs of iron-responsive elements (IREs) interacting with the iron-regulatory protein IRP1 (Supplementary Table S1).…”

“…The water temperature at the time of collection was and 0 + 2 • C (January), +4 + 5 • C (November) and +12 + 15 • C (August). The sampling was done in a way that sponges remained attached to the substrate (alga), allowing sponge regeneration [24]. Sponges were kept within 7-8 specimens in 5 L aquariums, natural seawater, 2-4 • C or 10-12 • C, and transported to the Koltzov Institute of Developmental Biology (Moscow, Russia).…”

“…Sponges (phylum Porifera) are benthic animals, and likely represent the oldest phylum of the existing Metazoa. Sea sponges of the sub-tidal zone are well adapted to changes in the temperature and oxygen content and provide a unique model for studying the cell adaptation processes in animals [24]. The sea sponges grow only in the presence of iron ions [25].…”

“…By using biochemical methods and transcriptomic analyses, we have previously described iron metabolic and heme biosynthesis/transport pathways and their association with the reaggregation process in two cold-water sea sponges of cl. Demospongia, Halisarca dujardini (lacking spicules) and Halichondria panicea (having spicules) [24,40]. In the present study, we analyze ferritin complexes of these two sponge species, along with their regulation at transcriptional/translational levels, and their contribution to the adaptation processes.…”

Mitochondrial Metal Ion Transport in Cell Metabolism and Disease

“…MFRN (SLC25A37) belongs to the vertebrate mitochondrial solute carrier protein family, which transports various metabolites and cofactors on the MIM. Some researchers show that the MFRN is a carrier of iron ions into mitochondria, and mitochondria of MFRN mutants disrupt iron ion uptake, leading to severe hypochromic anemia and stagnant red blood cell maturation [ 72 , 73 , 74 , 75 ]. In mouse embryonic stem cells, the lack of MFRN causes fibroblasts to stop maturing and inhibits heme synthesis [ 72 ].…”