Avian magnetoreception model realized by coupling a magnetite-based mechanism with a radical-pair-based mechanism

Many animal species have been proven to use the geomagnetic field for their navigation, but the biophysical mechanism of magnetoreception has remained enigmatic. In this paper, we present a special biophysical model that consists of magnetite-based and radical-pair-based mechanisms for avian magnetoreception. The amplitude of the resultant magnetic field around the magnetic particles corresponds to the geomagnetic field direction and affects the yield of singlet/triplet state products in the radical-pair reactions. Therefore, in the proposed model, the singlet/triplet state product yields are related to the geomagnetic field information for orientational detection. The resultant magnetic fields corresponding to two materials with different magnetic properties are analyzed under different geomagnetic field directions. The results show that ferromagnetic particles in organisms can provide more significant changes in singlet state products than superparam- agnetic particles, and the period of variation for the singlet state products with an included angle in the geomagnetic field is approximately 180 when the magnetic particles are ferromagnetic materials, consistent with the experimental results obtained from the avian magnetic compass. Further, the calculated results of the singlet state products in a reception plane show that the proposed model can explain the avian magnetoreception mechanism with an inclination compass.

On the evolutionary trail of MagRs

Magnetic sense,or termed magnetoreception,has evolved in a broad range of taxa within the animal kingdom to facilitate orientation and navigation.MagRs,highly conserved A-type iron-sulfur proteins,are widely distributed across all phyla and play essential roles in both magnetoreception and iron-sulfur cluster biogenesis.However,the evolutionary origins and functional diversification of MagRs from their prokaryotic ancestor remain unclear.In this study,MagR sequences from 131 species,ranging from bacteria to humans,were selected for analysis,with 23 representative sequences covering species from prokaryotes to Mollusca,Arthropoda,Osteichthyes,Reptilia,Aves,and mammals chosen for protein expression and purification.Biochemical studies revealed a gradual increase in total iron content in MagRs during evolution.Three types of MagRs were identified,each with distinct iron and/or iron-sulfur cluster binding capacity and protein stability,indicating continuous expansion of the functional roles of MagRs during speciation and evolution.This evolutionary biochemical study provides valuable insights into how evolution shapes the physical and chemical properties of biological molecules such as MagRs and how these properties influence the evolutionary trajectories of MagRs.

Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically

The ability to navigate long distances is essential for many animals to locate shelter,food,and breeding grounds.Magnetic sense has evolved in various migratory and homing species to orient them based on the geomagnetic field.A highly conserved ironsulfur cluster assembly protein IscA is proposed as an animal magnetoreceptor(MagR).Iron-sulfur cluster binding is also suggested to play an essential role in MagR magnetism and is thus critical in animal magnetoreception.In the current study,we provide evidence for distinct iron binding and iron-sulfur cluster binding in MagR in pigeons,an avian species that relies on the geomagnetic field for navigation and homing.Pigeon MagR showed significantly higher total iron content from both iron-and ironsulfur binding.Y65 in pigeon MagR was shown to directly mediate mononuclear iron binding,and its mutation abolished iron-binding capacity of the protein.Surprisingly,both iron binding and iron-sulfur binding demonstrated synergistic effects,and thus appear to be integral and indispensable to pigeon MagR magnetism.These results not only extend our current understanding of the origin and complexity of MagR magnetism,but also imply a possible molecular explanation for the huge diversity in animal magnetoreception.

Observations on a magnetotactic bacteria-grazing ciliate in sediment from the intertidal zone of Huiquan Bay,China

Magnetotactic bacteria(MTB)are a group of prokaryotes having the ability to orient and swim along geomagnetic field lines because they contain intracellular magnetosomes that are synthesized through a biomineralization process.Magnetosomes have recently also been found in unicellular eukaryotes,which are referred to as magnetically responsive protists(MRPs).The magnetosomes have three origins in MRPs.In this study,we characterized a MTB-grazing ciliated MRP that was magnetically collected from intertidal sediment of Huiquan Bay,Qingdao,China.Based on 18S rRNA gene sequence analysis,the ciliated MRP was tentatively identified as Uronemella parafi lificum HQ.Using transmission electron microscopy,we observed that magnetosomes having 2-3 shapes were randomly distributed within this ciliate.Energydispersive X-ray spectroscopy and high-resolution transmission electron microscopy images of the magnetosomes were consistent with them being composed of magnetite.Magnetosomes having the same shape and mineral composition were also detected in MTB that occurred in the same environment as the ciliated MRP.Statistical analysis showed that the size and shape of the magnetosomes in the ciliated MRP were similar to those in MTB.The results suggest that this ciliated MRP can graze,ingest,and digest various types of MTB.It is certainly worth noting that this is the first record of MRPs in Asian aquatic sediment and suggesting they might be widely distributed.These results also support the assertion that MRPs probably contribute to the ecological cycles of iron,and expand possibilities for research into the mechanism of magnetoreception in eukaryotes.

Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain

Magnetotactic bacteria(MTB),ubiquitous in soil and fresh and saltwater sources have been identified in the microbiome of humans and many animals.MTB endogenously produce magnetic nanocrystals enabling them to orient and navigate along geomagnetic fields.Similar magnetite deposits have been found throughout the tissues of the human brain,including brain regions associated with orientation such as the cerebellum and hippocampus,the origins of which remain unknown.Speculation over the role and source of MTB in humans,as well as any association with the brain,remain unanswered.We performed a metagenomic analysis of the gut microbiome of 34 healthy females as well as grey matter volume analysis in magnetite-rich brain regions associated with orientation and navigation with the goal of identifying specific MTB that could be associated with brain structure in orientation and navigation regions.We identified seven MTB in the human gut microbiome:Magnetococcus marinus,Magnetospira sp.QH-2,Magnetospirillum magneticum,Magnetospirillum sp.ME-1,Magnetospirillum sp.XM-1,Magnetospirillum gryphiswaldense,and Desulfovibrio magneticus.Our preliminary results show significant negative associations between multiple MTB with bilateral flocculonodular lobes of the cerebellum and hippocampus(adjusted for total intracranial volume,uncorrected P<0.05).These findings indicate that MTB in the gut are associated with grey matter volume in magnetite-rich brain regions related to orientation and navigation.These preliminary findings support MTB as a potential biogenic source for brain magnetite in humans.Further studies will be necessary to validate and elucidate the relationship between these bacteria,magnetite concentrations,and brain function.

Marine turtle hatchlings use multiple sensory cues to orient their crawling towards the sea:biological and conservation policy implications

The ability of sea turtle hatchlings to find the seashore soon after hatching is thought to be exclusively dependent upon visual information. Target-oriented movements in most vertebrates, however, relay on combining information gathered through different sensory systems. Hence, in this work, we investigated whether olfactory and/or magnetic information might complement visual cues during hatchling’s seaward crawling. Acute olfactory deprivation and distorted magnetic sensation in visually competent hatchlings resulted in a scattering of seaward crawling routes among cardinal points, some of them being different from those strongly preferred by control hatchlings. In addition, blindfolded hatchlings also displayed a striking misrouting while crawling on the beach surface in spite of having intact olfactory and magnetic senses. Together these results support the notion that visual information is crucial for seaward crawling, but also that olfactory and magnetic information complement visual cues when turtle hatchlings display this behavior. Hence, the present observations suggest that multisensory cues are used by turtle hatchlings while crawling towards the sea. This work also has important implications on the design of species conservation measures and policies. In the near future, efforts must be made to identify and preserve the local natural sources of odors and magnetic cues, in addition to preventing the perturbing effects of artificial lighting on adult and hatchling turtle crawling behavior.

Identification of zebrafish magnetoreceptor and cryptochrome homologs

Magnetoreception is essential for magnetic orientation in animal migration. The molecular basis for magnetoreception has re- cently been elucidated in fruitfly as complexes between the magnetic receptor magnetoreceptor （MagR） and its ligand crypto- chrome （Cry）. MagR and Cry are present in the animal kingdom. However, it is unknown whether they perform a conserved role in diverse animals. Here we report the identification and expression of zebrafish MagR and Cry homologs towards under- standing their roles in lower vertebrates. A single rnagr gene and 7 cry genes are present in the zebrafish genome. Zebrafish has four cryl genes （crylaa, crylab, crylba and cry]bb） homologous to human CRY1 and a single ortholog of human CRY2 as well as 2 cry-like genes （cry4 and cryS）. By RT-PCR, magr exhibited a high level of ubiquitous RNA expression in embryos and adult organs, whereas cry genes displayed differential embryonic and adult expression. Importantly, magr depletion did not produce apparent abnormalities in organogenesis. Taken together, magr and cry2 exist as a single copy gene, whereas cryl exists as multiple gene duplicates in zebrafish. Our result suggests that magr may play a dispensable role in organogenesis and predicts a possibility to generate rnagr mutants for analyzing its role in zebrafish.

Geomagnetic field absenee reduces adult body weight of a migratory insect by disrupt!ng feeding behavior and appetite regulation

The geomagnetic field(GMF)is well documented for its essential role as a cue used in animal orientation or navigation.Recent evidence indicates that the absence of GMF(mimicked by the near-zero magnetic field,NZMF)can trigger stress-like responses such as reduced body weight,as we have previously shown in the brown planthopper,Nilaparvata lugens.In this study,we found that consistent with the significantly decreased body weight of newly emerged female(—14.67%)and male(—13.17%)adult N.lugens,the duration of the phloem ingestion feeding waveform was significantly reduced by 32.02%in 5th instar nymphs reared under the NZMF versus GMF.Interestingly,5th instar nymphs that exhibited reduced feeding had significantly higher glucose levels(+16.98%and+20.05%;24 h and 48 h after molting),which are associated with food aversion,and expression patterns of their appetite-related neuropeptide genes(neuropeptide F,dow regulated overall;short neuropeptide F,dowregulated overall;adipokinetic hormone up-regulated overall;and adipokinetic hormone receptor,down-regulated overall)were also altered under the absence of GMF in a manner consistent with diminishing appetite.Moreover,the expressions of the potential magnetosensor croptochromes(Crys)were found significantly altered under the absence of GMF,indicating the likely upstream signaling of the Cry-mediated magnetoreception mechanisms.These findings support the hypothesis that strong changes in GMF intensity can reduce adult body weight through affecting insect feeding behavior and underlying regulatory processes including appetite regulation.Our results highlight that GMF could be necessary for the maintenanee of energy homeostasis in insects.

Experimental quantum simulation of Avian Compass in a nuclear magnetic resonance system

Avian magnetoreception is the capacity for avians to sense the direction of the Earth's magnetic field. Discovered more than forty years ago, it has attracted intensive studies over the years. One promising model for describing this capacity in avians is the widely used reference-and-probe model where radical pairs within the eyes of bird combines to form singlet and triplet quantum states.The yield depends on the angle between the Earth's magnetic field and the molecules' axis, hence the relative value of yield of the singlet state or triplet state enables avians to sense the direction. Here we report the experimental demonstration of avian magnetoreception in a nuclear magnetic resonance quantum information processor. It is shown clearly from the experiment that the yield of the singlet state attains maximum when it is normal to the Earth's magnetic field, and the experimental results agree with theory very well.

Identification of medaka magnetoreceptor and cryptochromes

Magnetoreception is a hallmark ability of animals for orientation and migration via sensing and utilizing geomagnetic fields.Magnetoreceptor(MagR) and cryptochromes(Cry) have recently been identified as the basis for magnetoreception in Drosophila.However,it has remained unknown whether MagR and Cry have conserved roles in diverse animals.Here we report the identification and expression of magr and cry genes in the fish medaka(Oryzias latipes).Cloning and sequencing identified a single magr gene,four cry genes and one cry-like gene in medaka.By sequence alignment,chromosomal synteny and gene structure analysis,medaka cry2 and magr were found to be the orthologs of human Cry2 and Magr,with cry1 aa and crylab being coorthologs of human Cry1.Therefore,magr and cry2 have remained as single copy genes,whereas cry1 has undergone two rounds of gene duplication in medaka.Interestingly,magr and cry genes were detected in various stages throughout embryogenesis and displayed ubiquitous expression in adult organs rather than specific or preferential expression in neural organs such as brain and eye.Importantly,magr knockdown by morpholino did not produce visible abnormality in developing embryos,pointing to the possibility of producing viable magr knockouts in medaka as a vertebrate model for magnet biology.