Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the Alphaproteobacteria

The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria

Classification of a Complexly Mixed Magnetic Mineral Assemblage in Pacific Ocean Surface Sediment by Electron Microscopy and Supervised Magnetic Unmixing

Unambiguous magnetic mineral identification in sediments is a prerequisite for reconstructing paleomagnetic and paleoenvironmental information from environmental magnetic parameters. We studied a deep-sea surface sediment sample from the Clarion Fracture Zone region, central Pacific Ocean, by combining magnetic measurements and scanning and transmission electron microscopic analyses. Eight titanomagnetite and magnetite particle types are recognized based on comprehensive documentation of crystal morphology, size, spatial arrangements, and compositions, which are indicative of their corresponding origins. Type-1 particles are detrital titanomagnetites with micron- and submicron sizes and irregular and angular shapes. Type-2 and -3 particles are well-defined octahedral titanomagnetites with submicron and nanometer sizes, respectively, which are likely related to local hydrothermal and volcanic activity. Type-4 particles are nanometer-sized titanomagnetites hosted within silicates, while type-5 particles are typical dendrite-like titanomagnetites that likely resulted from exsolution within host silicates. Type-6 particles are single domain magnetite magnetofossils related to local magnetotactic bacterial activity. Type-7 particles are superparamagnetic magnetite aggregates, while Type-8 particles are defect-rich single crystals composed of many small regions. Electron microscopy and supervised magnetic unmixing reveal that type-1 to -5 titanomagnetite and magnetite particles are the dominant magnetic minerals. In contrast, the magnetic contribution of magnetite magnetofossils appears to be small. Our work demonstrates that incorporating electron microscopic data removes much of the ambiguity associated with magnetic mineralogical interpretations in traditional rock magnetic measurements.This study was supported financially by the National Natural Science Foundation of China (Grant Nos. 41920104009, 41890843, and 41621004), The Senior User Project of RVKEXUE2019GZ06 (Center for Ocean Mega-Science, Chinese Academy of Sciences)

Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea

Multicellular magnetotactic prokaryotes (MMPs) are a group of aggregates composed of 7-45 gram-negative cells synthesizing intracellular magnetic crystals. Although they are thought to be globally distributed, MMPs have been observed only in marine environments in America and Europe. Most MMPs share a rosette-like morphology and biomineralize iron sulfide crystals. In the present study, abundant MMPs were observed, with a density of 26 ind./cm(3), in the sediments of a coastal lagoon, Lake Yuehu, in the Yellow Sea. Optical microscopy showed that all of them were rosette shaped with a diameter of 5.5+/-0.8 mu m. Transmission electron microscopy revealed that these MMPs were composed of 10-16 ovoid cells and flagellated peritrichously. High-resolution transmission electron microscopy and energy dispersive X-ray analysis indicated that they biomineralized bullet-shaped magnetite crystals in highly organized parallel chains within which the magnetosomes were oriented in the same direction. This is the first report of MMPs from Asia and demonstrates the ubiquitous distribution of MMPs.Multicellular magnetotactic prokaryotes (MMPs) are a group of aggregates composed of 7-45 gram-negative cells synthesizing intracellular magnetic crystals. Although they are thought to be globally distributed, MMPs have been observed only in marine environments in America and Europe. Most MMPs share a rosette-like morphology and biomineralize iron sulfide crystals. In the present study, abundant MMPs were observed, with a density of 26 ind./cm(3), in the sediments of a coastal lagoon, Lake Yuehu, in the Yellow Sea. Optical microscopy showed that all of them were rosette shaped with a diameter of 5.5+/-0.8 mu m. Transmission electron microscopy revealed that these MMPs were composed of 10-16 ovoid cells and flagellated peritrichously. High-resolution transmission electron microscopy and energy dispersive X-ray analysis indicated that they biomineralized bullet-shaped magnetite crystals in highly organized parallel chains within which the magnetosomes were oriented in the same direction. This is the first report of MMPs from Asia and demonstrates the ubiquitous distribution of MMPs

Insight into the metabolic potential and ecological function of a novel Magnetotactic Nitrospirota in coral reef habitat

Magnetotactic bacteria (MTB) within the Nitrospirota phylum play important roles in biogeochemical cycles due to their outstanding ability to biomineralize large amounts of magnetite magnetosomes and intracellular sulfur globules. For several decades, Nitrospirota MTB were believed to only live in freshwater or low-salinity environments. While this group have recently been found in marine sediments, their physiological features and ecological roles have remained unclear. In this study, we combine electron microscopy with genomics to characterize a novel population of Nitrospirota MTB in a coral reef area of the South China Sea. Both phylogenetic and genomic analyses revealed it as representative of a novel genus, named as Candidatus Magnetocorallium paracelense XS-1. The cells of XS-1 are small and vibrioid-shaped, and have bundled chains of bullet-shaped magnetite magnetosomes, sulfur globules, and cytoplasmic vacuole-like structures. Genomic analysis revealed that XS-1 has the potential to respire sulfate and nitrate, and utilize the Wood–Ljungdahl pathway for carbon fixation. XS-1 has versatile metabolic traits that make it different from freshwater Nitrospirota MTB, including Pta-ackA pathway, anaerobic sulfite reduction, and thiosulfate disproportionation. XS-1 also encodes both the cbb3-type and the aa3-type cytochrome c oxidases, which may function as respiratory energy-transducing enzymes under high oxygen conditions and anaerobic or microaerophilic conditions, respectively. XS-1 has multiple copies of circadian related genes in response to variability in coral reef habitat. Our results implied that XS-1 has a remarkable plasticity to adapt the environment and can play a beneficial role in coral reef ecosystems

Genomic analysis of a pure culture of magnetotactic bacterium Terasakiella sp. SH-1

International audienceMagnetotactic bacteria (MTB) display magnetotaxis ability because of biomineralization of intracellular nanometer-sized, membrane-bound organelles termed magnetosomes. Despite having been discovered more than half a century, only a few representatives of MTB have been isolated and cultured in the laboratory. In this study, we report the genomic characterization of a novel marine magnetotactic spirillum strain SH-1 belonging to the genus Terasakiella that was recently isolated. A gene encoding haloalkane dehalogenase, which is involved in the degradation of chlorocyclohexane, chlorobenzene, chloroalkane and chloroalkene, was identified. SH-1 genome contained cysCHI and soxBAZYX genes, thus potentially capable of assimilatory sulfate reduction to H2S and using thiosulfate as electron donors and oxidizing it to sulfate. Genome of SH-1 also contained genes encoding periplasmic dissimilatory nitrate reductases (napAB), assimilatory nitrate reductase (nasA) and assimilatory nitrite reductases (nasB), suggesting that it is capable of gaining energy by converting nitrate to ammonia. The pure culture of Terasakiella sp. SH-1 together with its genomic results offers new opportunities to examine biology, physiology and biomineralization mechanisms of MTB

A species of magnetotactic deltaproteobacterium was detected at the highest abundance during an algal bloom

International audienceMagnetotactic bacteria (MTB) are a group of microorganisms that have the ability to synthesize intracellular magnetic crystals (magnetosomes). They prefer microaerobic or anaerobic aquatic sediments. Thus, there is growing interest in their ecological roles in various habitats. In this study we found co-occurrence of a large rod-shaped deltaproteobacterial magnetotactic bacterium (tentatively named LR-1) in the sediment of a Downloaded from https://academic.oup.com/femsle/advance-article-abstract/doi/10.1093/femsle/fnz253/5681391 by guest on 23 December 201

Diversity and Characterization of Multicellular Magnetotactic Prokaryotes From Coral Reef Habitats of the Paracel Islands, South China Sea

International audienceWhile multicellular magnetotactic prokaryotes (MMPs) are ubiquitous in marine environments, the diversity of MMPs in sediments of coral reef ecosystems has rarely been reported. In this study, we made an investigation on the diversity and characteristics of MMPs in sediments at 11 stations in coral reef habitats of the Paracel Islands. The results showed that MMPs were present at nine stations, with spherical mulberry-like MMPs (s-MMPs) found at all stations and ellipsoidal pineapple-like MMPs (e-MMPs) found at seven stations. The maximum abundance of MMPs was 6 ind./cm 3. Phylogenetic analysis revealed the presence of one e-MMP species and five s-MMP species including two species of a new genus. The results indicate that coral reef habitats of the Paracel Islands have a high diversity of MMPs that bio-mineralize multiple intracellular chains of iron crystals and play important role in iron cycling in such oligotrophic environment. These observations provide new perspective of the diversity of MMPs in general and expand knowledge of the occurrence of MMPs in coral reef habitats

Copper phosphide decorated g-C₃N₄ catalysts for highly efficient photocatalytic H₂ evolution

Designing functional heterojunctions to enhance photocatalytic hydrogen evolution is still a key challenge in the field of efficient solar energy utilization. Copper phosphides become an ideal material to serve as the cocatalysts during photocatalytic hydrogen evolution by virtue of the lower prices. In this study, we synthesized graphitic carbon nitride (g-C3N4) based catalysts loaded with copper phosphide (Cu3P, Cu97P3), which exhibit superior performance in photocatalytic H2 evolution. Ultraviolet (UV)-visible spectroscopy illustrated that the absorption of light strengthened after the loading of copper phosphide, and the time-resolved transient photoluminescence (PL) spectra showed that the separation and transfer of the photoexcited carriers greatly improved. Moreover, both copper phosphide/g-C3N4 photocatalysts exhibited a relatively high H2 evolution rate: Cu3P/g-C3N4 (maximum 343 μmol h-1 g-1), Cu97P3/g-C3N4 (162.9 μmol h-1 g-1) while copper phosphide themself exhibit no photocatalytic activity. Thus, the copper phosphides (Cu3P, Cu97P3) work as a cocatalyst during photocatalytic H2 evolution. The cycling experiments illustrated that both copper phosphide/g-C3N4 photocatalysts perform excellent stability in the photocatalytic H2 evolution. It is worth noting that while the NaH2PO2 was heated in the tube furnace for phosphorization to obtain Cu3P, the excessive PH3 could pass through the solution of CuSO4 to obtain Cu97P3 at the same time, which significantly improved the utilization of PH3 and reduced the risk of toxicity. This work could provide new strategies to design photocatalysts decorated with copper phosphide for highly efficient visible-light-driven hydrogen evolution.This work was financially supported by the National Natural Science Foundation of China (Grant No. 52103339), Natural Science Foundation of Hubei Province (Grant No. 2018CFB282) and Science Foundation of Hubei University of Technology (Grant No. BSQD2017065)

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

International audienceMagnetotactic bacteria (MTB) are a group of prokaryotes having the ability to orient and swim along geomagnetic field lines because they contain intracellular magnetosomes, which 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, China. Based on 18S rRNA gene sequence analysis, the ciliated MRP was tentatively identified as Uronemella parafilificum HQ. Using transmission electron microscopy, we observed that magnetosomes having 2-3 shapes were randomly distributed within this ciliate. Energy-dispersive 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

A Novel Isolate of Spherical Multicellular Magnetotactic Prokaryotes Has Two Magnetosome Gene Clusters and Synthesizes Both Magnetite and Greigite Crystals

International audienceMulticellular magnetotactic prokaryotes (MMPs) are a unique group of magnetotactic bacteria that are composed of 10–100 individual cells and show coordinated swimming along magnetic field lines. MMPs produce nanometer-sized magnetite (Fe3O4) and/or greigite (Fe3S4) crystals—termed magnetosomes. Two types of magnetosome gene cluster (MGC) that regulate biomineralization of magnetite and greigite have been found. Here, we describe a dominant spherical MMP (sMMP) species collected from the intertidal sediments of Jinsha Bay, in the South China Sea. The sMMPs were 4.78 ± 0.67 μm in diameter, comprised 14–40 cells helical symmetrically, and contained bullet-shaped magnetite and irregularly shaped greigite magnetosomes. Two sets of MGCs, one putatively related to magnetite biomineralization and the other to greigite biomineralization, were identified in the genome of the sMMP, and two sets of paralogous proteins (Mam and Mad) that may function separately and independently in magnetosome biomineralization were found. Phylogenetic analysis indicated that the sMMPs were affiliated with Deltaproteobacteria. This is the first direct report of two types of magnetosomes and two sets of MGCs being detected in the same sMMP. The study provides new insights into the mechanism of biomineralization of magnetosomes in MMPs, and the evolutionary origin of MGCs