Elongation capacity of polyunsaturated fatty acids in the annelid Platynereis dumerilii.

Elongation of very long-chain fatty acid (Elovl) proteins plays pivotal functions in the biosynthesis of the physiologically essential long-chain polyunsaturated fatty acids (LC-PUFA). Polychaetes have important roles in marine ecosystems, contributing not only to nutrient recycling but also exhibiting a distinctive capacity for biosynthesizing LC-PUFA. To expand our understanding of the LC-PUFA biosynthesis in polychaetes, this study conducted a thorough molecular and functional characterization of Elovl occurring in the model organism Platynereis dumerilii. We identify six Elovl in the genome of P. dumerilii. The sequence and phylogenetic analyses established that four Elovl, identified as Elovl2/5, Elovl4 (two genes) and Elovl1/7, have putative functions in LC-PUFA biosynthesis. Functional characterization confirmed the roles of these elongases in LC-PUFA biosynthesis, demonstrating that P. dumerilii possesses a varied and functionally diverse complement of Elovl that, along with the enzymatic specificities of previously characterized desaturases, enables P. dumerilii to perform all the reactions required for the biosynthesis of the LC-PUFA. Importantly, we uncovered that one of the two Elovl4-encoding genes is remarkably long in comparison with any other animals' Elovl, which contains a C terminal KH domain unique among Elovl. The distinctive expression pattern of this protein in photoreceptors strongly suggests a central role in vision.

Is there potential for estradiol receptor signaling in lophotrochozoans?

Estrogen receptors (ERs) are thought to be the ancestor of all steroid receptors and are present in most lophotrochozoans studied to date, including molluscs, annelids, and rotifers. A number of studies have investigated the functional role of estrogen receptors in invertebrate species, although most are in molluscs, where the receptor is constitutively active. In vitro experiments provided evidence for ligand-activated estrogen receptors in annelids, raising important questions about the role of estrogen signalling in lophotrochozoan lineages. Here, we review the concordant and discordant evidence of estradiol receptor signalling in lophotrochozoans, with a focus on annelids and rotifers. We explore the de novo synthesis of estrogens, the evolution and expression of estrogen receptors, and physiological responses to activation of estrogen receptors in the lophotrochozoan phyla Annelida and Rotifera. Key data are missing to determine if de novo biosynthesis of estradiol in non-molluscan lophotrochozoans is likely. For example, an ortholog for the CYP11 gene is present, but confirmation of substrate conversion and measured tissue products is lacking. Orthologs CYP17 and CYP19 are lacking, yet intermediates or products (e.g. estradiol) in tissues have been measured. Estrogen receptors are present in multiple species, and for a limited number, in vitro data show agonist binding of estradiol and/or transcriptional activation. The expression patterns of the lophotrochozoan ERs suggest developmental, reproductive, and digestive roles but are highly species dependent. E2 exposures suggest that lophotrochozoan ERs may play a role in reproduction, but no strong dose-response relationship has been established. Therefore, we expect most lophotrochozoan species, outside of perhaps platyhelminths, to have an ER but their physiological role remains elusive. Mining genomes for orthologs gene families responsible for steroidogenesis, coupled with in vitro and in vivo studies of the steroid pathway are needed to better assess whether lophotrochozoans are capable of estradiol biosynthesis. One major challenge is that much of the data are divided across a diversity of species. We propose that the polychaetes Capitella teleta or Platyneris dumerilii, and rotifer Brachionus manjavacas may be strong species choices for studies of estrogen receptor signalling, because of available genomic data, established laboratory culture techniques, and gene knockout potential.

Functionally diverse front-end desaturases are widespread in the phylum Annelida.

Aquatic single-cell organisms have long been believed to be unique primary producers of omega-3 long-chain (≥C20) polyunsaturated fatty acids (ω3 LC-PUFA). Multiple invertebrates including annelids have been discovered to possess methyl-end desaturases enabling key steps in the de novo synthesis of ω3 LC-PUFA, and thus potentially contributing to their production in the ocean. Along methyl-end desaturases, the repertoire and function of further LC-PUFA biosynthesising enzymes is largely missing in Annelida. In this study we examined the front-end desaturase gene repertoire across the phylum Annelida, from Polychaeta and Clitellata, major classes of annelids comprising most annelid diversity. We further characterised the functions of the encoded enzymes in selected representative species by using a heterologous expression system based in yeast, demonstrating that functions of Annelida front-end desaturases have highly diversified during their expansion in both terrestrial and aquatic ecosystems. We concluded that annelids possess at least two front-end desaturases with Δ5 and Δ6Δ8 desaturase regioselectivities, enabling all the desaturation reactions required to convert the C18 precursors into the physiologically relevant LC-PUFA such as eicosapentaenoic and arachidonic acids, but not docosahexaenoic acid. Such a gene complement is conserved across the different taxonomic groups within Annelida.

De novo phytosterol synthesis in animals.

Sterols are vital for nearly all eukaryotes. Their distribution differs in plants and animals, with phytosterols commonly found in plants whereas most animals are dominated by cholesterol. We show that sitosterol, a common sterol of plants, is the most abundant sterol in gutless marine annelids. Using multiomics, metabolite imaging, heterologous gene expression, and enzyme assays, we show that these animals synthesize sitosterol de novo using a noncanonical C-24 sterol methyltransferase (C24-SMT). This enzyme is essential for sitosterol synthesis in plants, but not known from most bilaterian animals. Our phylogenetic analyses revealed that C24-SMTs are present in representatives of at least five animal phyla, indicating that the synthesis of sterols common to plants is more widespread in animals than currently known.

Morphological and molecular features of early regeneration in the marine annelid Ophryotrocha xiamen.

Regeneration capability varies in the phylum Annelida making them an excellent group to investigate the differences between closely related organisms. Several studies have described the process of regeneration, while the underlying molecular mechanism remains unclear, especially during the early stage (wound healing and blastema formation). In this study, the newly identified Ophryotrocha xiamen was used to explore the early regeneration. The detailed morphological and molecular analyses positioned O. xiamen within 'labronica' clade. We analyzed the morphological changes during regeneration process (0-3 days post amputation) and molecular changes during the early regeneration stage (1 day post amputation). Wound healing was achieved within one day and a blastema formed one day later. A total of 243 DEGs were mainly involved in metabolism and signal transduction. Currently known regeneration-related genes were identified in O. xiamen which could help with exploring the functions of genes involved in regeneration processes. According to their conserved motif, we identified 8 different Hox gene fragments and Hox5 and Lox2 were found to be absent in early regeneration and during regular growth. Our data can promote further use of O. xiamen which can be used as an experimental model for resolving crucial problems of developmental biology in marine invertebrates.

Diverse Localization Patterns of an R-Type Lectin in Marine Annelids.

Lectins facilitate cell-cell contact and are critical in many cellular processes. Studying lectins may help us understand the mechanisms underlying tissue regeneration. We investigated the localization of an R-type lectin in a marine annelid (Perinereis sp.) with remarkable tissue regeneration abilities. Perinereis nuntia lectin (PnL), a galactose-binding lectin with repeating Gln-X-Trp motifs, is derived from the ricin B-chain. An antiserum was raised against PnL to specifically detect a 32-kDa lectin in the crude extracts from homogenized lugworms. The antiserum detected PnL in the epidermis, setae, oblique muscle, acicula, nerve cord, and nephridium of the annelid. Some of these tissues and organs also produced Galactose (Gal) or N-acetylgalactosamine (GalNAc), which was detected by fluorescent-labeled plant lectin. These results indicated that the PnL was produced in the tissues originating from the endoderm, mesoderm, and ectoderm. Besides, the localizing pattern of PnL partially merged with the binding pattern of a fluorescent-labeled mushroom lectin that binds to Gal and GalNAc. It suggested that PnL co-localized with galactose-containing glycans in Annelid tissue; this might be the reason PnL needed to be extracted with haptenic sugar, such as d-galactose, in the buffer. Furthermore, we found that a fluorescein isothiocyanate-labeled Gal/GalNAc-binding mushroom lectin binding pattern in the annelid tissue overlapped with the localizing pattern of PnL. These findings suggest that lectin functions by interacting with Gal-containing glycoconjugates in the tissues.

Structural and Functional Characterization of the FGF Signaling Pathway in Regeneration of the Polychaete Worm Alitta virens (Annelida, Errantia).

Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of Alitta virens. For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians.

The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata).

Bloodfeeding is employed by many parasitic animals and requires specific innovations for efficient feeding. Some of these innovations are molecular features that are related to the inhibition of hemostasis. For example, bloodfeeding insects, bats, and leeches release proteins with anticoagulatory activity through their salivary secretions. The antistasin-like protein family, composed of serine protease inhibitors with one or more antistasin-like domains, is tightly linked to inhibition of hemostasis in leeches. However, this protein family has been recorded also in non-bloodfeeding invertebrates, such as cnidarians, mollusks, polychaetes, and oligochaetes. The present study aims to 1) root the antistasin-like gene tree and delimit the major orthologous groups, 2) identify potential independent origins of salivary proteins secreted by leeches, and 3) identify major changes in domain and/or motif structure within each orthologous group. Five clades containing leech antistasin-like proteins are distinguishable through rigorous phylogenetic analyses based on nine new transcriptomes and a diverse set of comparative data: the trypsin + leukocyte elastase inhibitors clade, the antistasin clade, the therostasin clade, and two additional, unnamed clades. The antistasin-like gene tree supports multiple origins of leech antistasin-like proteins due to the presence of both leech and non-leech sequences in one of the unnamed clades, but a single origin of factor Xa and trypsin + leukocyte elastase inhibitors. This is further supported by three sequence motifs that are exclusive to antistasins, the trypsin + leukocyte elastase inhibitor clade, and the therostasin clade, respectively. We discuss the implications of our findings for the evolution of this diverse family of leech anticoagulants.

Black spicules from a new interstitial opheliid polychaete Thoracophelia minuta sp. nov. (Annelida: Opheliidae).

The phylum Annelida exhibits high morphological diversity coupled with its extensive ecological diversity, and the process of its evolution has been an attractive research subject for many researchers. Its representatives are also extensively studied in fields of ecology and developmental biology and important in many other biology related disciplines. The study of biomineralisation is one of them. Some annelid groups are well known to form calcified tubes but other forms of biomineralisation are also known. Herein, we report a new interstitial annelid species with black spicules, Thoracophelia minuta sp. nov., from Yoichi, Hokkaido, Japan. Spicules are minute calcium carbonate inclusions found across the body and in this new species, numerous black rod-like inclusions of calcium-rich composition are distributed in the coelomic cavity. The new species can be distinguished from other known species of the genus by these conspicuous spicules, shape of branchiae and body formula. Further, the new species' body size is apparently smaller than its congeners. Based on our molecular phylogenetic analysis using 18S and 28S sequences, we discuss the evolutionary significance of the new species' spicules and also the species' progenetic origin.

Oxygen consumption during and post-hypoxia exposure in bearded fireworms (Annelida: Amphinomidae).

Oxygen is necessary for all marine animals to support metabolic functions. When chronic low dissolved oxygen (DO) conditions occur, organisms must adjust to overcome this stressor's effect on metabolic rates. The bearded fireworm, Hermodice carunculata, is a widespread species frequently exposed to hypoxic conditions in areas within its broad distribution which may impact metabolism, wound healing, and regeneration. To study the impact of hypoxia on their metabolic rates, we exposed fireworms to two levels of lower than normal DO conditions (low 2.5 ± 0.25 mg O2 L-1 and mid 4.5 ± 0.25 mg O2 L-1) for 7 days by pumping nitrogen into their holding tanks. During a chronic hypoxia trial, we quantified oxygen consumption in each experimental group and subsequently determined post-hypoxia oxygen consumption of individuals from the lowest oxygen level. During the hypoxic exposure, the oxygen uptake rates declined in low and mid DO conditions, while remaining relatively constant for the normoxic (7.0 ± 0.25 mg O2 L-1) control. We then compared the oxygen consumption rates from the lowest DO condition to fireworms likely never exposed to hypoxia and fireworms from a location likely to be exposed to hypoxia. We found higher oxygen consumption rates in the experimentally hypoxia-exposed worms. These results suggest prolonged negative impacts of hypoxic exposure, leading to a lasting elevation of metabolic rates of these marine invertebrates. The increase in metabolic rates may lead to increased predation on their prey of choice, economically and commercially important coral, causing increased degradation of already threatened coral reef ecosystems.

Ultrastructure of Ediacaran cloudinids suggests diverse taphonomic histories and affinities with non-biomineralized annelids.

Cloudinids have long been considered the earliest biomineralizing metazoans, but their affinities have remained contentious and undetermined. Based on well-preserved ultrastructures of two taxa, we here propose new interpretations regarding both their extent of original biomineralization and their phylogenetic affinity. One of these taxa is a new cloudinid from Mongolia, Zuunia chimidtsereni gen. et sp. nov., which exhibits key characteristics of submicrometric kerogenous lamellae, plastic tube-wall deformation, and tube-wall delamination. Multiple carbonaceous lamellae are also discovered in Cloudina from Namibia and Paraguay, which we interpret to have originated from chitinous or collagenous fabrics. We deduce that these cloudinids were predominantly originally organic (chitinous or collagenous), and postmortem decay and taphonomic mineralization resulted in the formation of aragonite and/or calcite. Further, based on our ultrastructural characterization and other morphological similarities, we suggest that the cloudinids should most parsimoniously be assigned to annelids with originally organic tubes.

Functional role of pax6 during eye and nervous system development in the annelid Capitella teleta.

The transcription factor Pax6 is an important regulator of early animal development. Loss of function mutations of pax6 in a range of animals result in a reduction or complete loss of the eye, a reduction of a subset of neurons, and defects in axon growth. There are no studies focusing on the role of pax6 during development of any lophotrochozoan representative, however, expression of pax6 in the developing eye and nervous system in a number of species suggest that pax6 plays a highly conserved role in eye and nervous system formation. We investigated the functional role of pax6 during development of the marine annelid Capitella teleta. Expression of pax6 transcripts in C. teleta larvae is similar to patterns found in other animals, with distinct subdomains in the brain and ventral nerve cord as well as in the larval and juvenile eye. To perturb pax6 function, two different splice-blocking morpholinos and a translation-blocking morpholino were used. Larvae resulting from microinjections with either splice-blocking morpholino show a reduction of the pax6 transcript. Development of both the larval eyes and the central nervous system architecture are highly disrupted following microinjection of each of the three morpholinos. The less severe phenotype observed when only the homeodomain is disrupted suggests that presence of the paired domain is sufficient for partial function of the Pax6 protein. Preliminary downstream target analysis confirms disruption in expression of some components of the retinal gene regulatory network, as well as disruption of genes involved in nervous system development. Results from this study, taken together with studies from other species, reveal an evolutionarily conserved role for pax6 in eye and neural specification and development.

Siboglinids (Annelida, Siboglinidae) as Possible Hydrocarbon Indicators as Exemplified by the Sea of Okhotsk.

The geographic and bathymetric distribution of siboglinids in the Sea of Okhotsk was studied. At least 75% of all siboglinid findings were at a depth up to 400 m. Most of them were concentrated in the northwestern part of the shelf. Comparison of the data on siboglinid distribution in the Sea of Okhotsk and the aggregate geological data on hydrocarbon distribution showed that, in the Sea of Okhotsk, siboglinids were mostly in the regions of hydrocarbon manifestations, but they were absent in the central areas with the minimum methane and hydrocarbon concentrations in both benthic sediments and the uppermost water layers.

Desiccation tolerance: an unusual window into stress biology.

Climate change has accentuated the importance of understanding how organisms respond to stresses imposed by changes to their environment, like water availability. Unusual organisms, called anhydrobiotes, can survive loss of almost all intracellular water. Desiccation tolerance of anhydrobiotes provides an unusual window to study the stresses and stress response imposed by water loss. Because of the myriad of stresses that could be induced by water loss, desiccation tolerance seemed likely to require many established stress effectors. The sugar trehalose and hydrophilins (small intrinsically disordered proteins) had also been proposed as stress effectors against desiccation because they were found in nearly all anhydrobiotes, and could mitigate desiccation-induced damage to model proteins and membranes in vitro. Here, we summarize in vivo studies of desiccation tolerance in worms, yeast, and tardigrades. These studies demonstrate the remarkable potency of trehalose and a subset of hydrophilins as the major stress effectors of desiccation tolerance. They act, at least in part, by limiting in vivo protein aggregation and loss of membrane integrity. The apparent specialization of individual hydrophilins for desiccation tolerance suggests that other hydrophilins may have distinct roles in mitigating additional cellular stresses, thereby defining a potentially new functionally diverse set of stress effectors.

The Sperm Proteome of the Echiuran Urechis unicinctus (Annelida, Echiura).

Sperm proteins presumably play critical roles in reproduction, but in many non-model animals their identities are unknown. A total of 147 sperm proteins from the echiuran worm Urechis unicinctus, the first sperm proteome in the phylum Annelida, are reported. The echiuran sperm proteome can be classified into diverse functional groups: energy metabolism (31%), protein synthesis and degradation (18%), spermatogenesis and sperm motility (12%), signal pathway (11%), ion channel and transport proteins (6%), cytoskeleton (4%), immunity and stress responses (3%), and fertilization (1%). These results will facilitate studies of mechanisms of fertilization in echiurans, as well as comparative studies of reproduction and evolution across lophotrochozoans. Data are available via ProteomeXchange with identifier PXD009176.

Regeneration of the germline in the annelid Capitella teleta.

The germline is essential for sexual reproduction and survival of the species. In many metazoans, the developmental potential to generate a distinct germline is segregated from somatic cell lineages early in embryogenesis, suggesting that the unique features of the germline must be established from its onset. Previous studies suggest that germ cells cannot regenerate once removed from the embryo, but few animals have been experimentally tested. We investigated the ability of the germline to regenerate in a lophotrochozoan, the segmented worm Capitella teleta, which has a stereotyped cell lineage program by deleting the germline precursor (cell 3D) in early stage embryos using an infrared laser. Larvae and juveniles resulting from germline deletions were examined for presence of multipotent progenitor cells (MPCs), stem cells that form the germ cells and somatic stem cells. In contrast to control deletions of a non-germline macromere, most larvae resulting from deletion of cell 3D lacked MPCs as assayed by expression of germline markers CapI-vasa, CapI-nanos and Ct-piwi1, but showed persistent expression of these markers in the somatic posterior growth zone. However, approximately 13% of experimental larvae had MPCs, indicative of some germline regeneration. In contrast, by two weeks post-metamorphosis, all juveniles resulting from deletion of cell 3D had MPCs, as detected by CapI-vasa expression. Furthermore, when raised to adulthood, most animals developed reproductive structures and were fertile. In another set of deletions, both the D quadrant mesodermal and germline progenitors were removed. These juveniles also regenerated MPCs. Surprisingly, this deletion caused substantial ectopic expression of CapI-vasa and CapI-nanos in other larval tissues. Our results indicate that C. teleta can regenerate the germline following removal of the germline progenitors in the early embryo. The dramatic difference in ability to regenerate the germline between the larval and adult stages suggests that there are two distinct compensation events at two phases of the life cycle: a regulative event in the early stage larva and a stem cell transition event after metamorphosis, when the animals are capable of substantial body regeneration.

Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome.

Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution and comparative physiology of luqin-type neuropeptide signalling, which has been characterised previously in protostomian invertebrates. Phylogenetic analysis indicates that luqin-type receptors and tachykinin-type receptors are paralogous and probably originated in a common ancestor of the Bilateria. In the deuterostomian lineage, luqin-type signalling has been lost in chordates but interestingly it has been retained in ambulacrarians. Therefore, here we characterised luqin-type signalling for the first time in an ambulacrarian - the starfish Asterias rubens (phylum Echinodermata). A luqin-like neuropeptide with a C-terminal RWamide motif (ArLQ; EEKTRFPKFMRW-NH2) was identified as the ligand for two luqin-type receptors in A. rubens, ArLQR1 and ArLQR2. Furthermore, analysis of the expression of the ArLQ precursor using mRNA in situ hybridisation revealed expression in the nervous system, digestive system and locomotory organs (tube feet) and in vitro pharmacology revealed that ArLQ causes dose-dependent relaxation of tube feet. Accordingly, previous studies have revealed that luqin-type signalling regulates feeding and locomotor activity in protostomes. In conclusion, our phylogenetic analysis combined with characterisation of luqin-type signalling in a deuterostome has provided new insights into neuropeptide evolution and function in the animal kingdom.

The ancestral retinoic acid receptor was a low-affinity sensor triggering neuronal differentiation.

Retinoic acid (RA) is an important intercellular signaling molecule in vertebrate development, with a well-established role in the regulation of hox genes during hindbrain patterning and in neurogenesis. However, the evolutionary origin of the RA signaling pathway remains elusive. To elucidate the evolution of the RA signaling system, we characterized RA metabolism and signaling in the marine annelid Platynereis dumerilii, a powerful model for evolution, development, and neurobiology. Binding assays and crystal structure analyses show that the annelid retinoic acid receptor (RAR) binds RA and activates transcription just as vertebrate RARs, yet with a different ligand-binding pocket and lower binding affinity, suggesting a permissive rather than instructive role of RA signaling. RAR knockdown and RA treatment of swimming annelid larvae further reveal that the RA signal is locally received in the medial neuroectoderm, where it controls neurogenesis and axon outgrowth, whereas the spatial colinear hox gene expression in the neuroectoderm remains unaffected. These findings suggest that one early role of the new RAR in bilaterian evolution was to control the spatially restricted onset of motor and interneuron differentiation in the developing ventral nerve cord and to indicate that the regulation of hox-controlled anterior-posterior patterning arose only at the base of the chordates, concomitant with a high-affinity RAR needed for the interpretation of a complex RA gradient.

Duplicated FoxA genes in the leech Helobdella: Insights into the evolution of direct development in clitellate annelids.

BACKGROUND: As an adaptation to the land, the clitellate annelid had reorganized its embryogenesis to develop "directly" without the ancestral planktonic larval stage. To study the evolution of gut development in the directly developing clitellates, we characterized the expression pattern of the conserved gut gene, FoxA, in the embryonic development of the leech. RESULTS: The leech has three FoxA paralogs. Hau-FoxA1 is first expressed in a subset of endoderm cells and then in the foregut and the midgut. Hau-FoxA2 is expressed in the stomodeum, which is secondarily derived from the anterior ectoderm in the clitellates rather than the tissue around the blastopore, the ancestral site of mouth formation in Phylum Annelida. Hau-FoxA3 is expressed during the morphogenesis of segmental ganglia from the ectodermal teloblast lineages, a clitellate-specific trait. Hau-FoxA1 and Hau-FoxA2 are also expressed during the morphogenesis of the leech-specific front sucker. CONCLUSIONS: The expression patterns suggested that Hau-FoxA1 carries out most of the conserved function in the endoderm and gut development, while the other two duplicates appear to have evolved unique novel functions in the directly developing clitellate embryos. Therefore, neofunctionalization and co-option of FoxA might have made a significant contribution to the evolution of direct development in Clitellata. Developmental Dynamics 247:763-778, 2018. © 2018 Wiley Periodicals, Inc.

First biochemical and crystallographic characterization of a fast-performing ferritin from a marine invertebrate.

Ferritin, a multimeric cage-like enzyme, is integral to iron metabolism across all phyla through the sequestration and storage of iron through efficient ferroxidase activity. While ferritin sequences from ∼900 species have been identified, crystal structures from only 50 species have been reported, the majority from bacterial origin. We recently isolated a secreted ferritin from the marine invertebrate Chaetopterus sp. (parchment tube worm), which resides in muddy coastal seafloors. Here, we present the first ferritin from a marine invertebrate to be crystallized and its biochemical characterization. The initial ferroxidase reaction rate of recombinant Chaetopterus ferritin (ChF) is 8-fold faster than that of recombinant human heavy-chain ferritin (HuHF). To our knowledge, this protein exhibits the fastest catalytic performance ever described for a ferritin variant. In addition to the high-velocity ferroxidase activity, ChF is unique in that it is secreted by Chaetopterus in a bioluminescent mucus. Previous work has linked the availability of Fe2+ to this long-lived bioluminescence, suggesting a potential function for the secreted ferritin. Comparative biochemical analyses indicated that both ChF and HuHF showed similar behavior toward changes in pH, temperature, and salt concentration. Comparison of their crystal structures shows no significant differences in the catalytic sites. Notable differences were found in the residues that line both 3-fold and 4-fold pores, potentially leading to increased flexibility, reduced steric hindrance, or a more efficient pathway for Fe2+ transportation to the ferroxidase site. These suggested residues could contribute to the understanding of iron translocation through the ferritin shell to the ferroxidase site.