Populations Of Magnetotactic Bacteria Research Articles

Paleoenvironmental Controls on the Abundances of Magnetofossils in the Southwestern Iberian Margin

AbstractMagnetofossils are nanosized magnetic fossil remnants of magnetotactic bacteria (MTB) that are widely distributed in marine and freshwater sediments. Past studies have revealed that changes in the morphology and abundance of magnetofossils are linked with diverse paleoenvironmental changes, such as glacial‐interglacial variation, redox conditions associated with primary productivity and organic matter supply, chemical weathering and diagenesis. Besides, it has long been speculated that changes in geomagnetic field intensity could also affect the abundance of magnetofossils. However, it is not yet clear, how these environmental factors controlled past MTB populations in combination. To answer this question, we studied magnetofossils‐rich sediments from cores MD01‐2443 and 2444 off the Southwest Iberian Margin. The paleomagnetic records of our samples reveal geomagnetic excursions corresponding to the Laschamp, Blake, Iceland Basin, and Pringle Falls events. We estimated the relative abundance of magnetofossils in the samples based on isothermal remanent magnetization unmixing and found it to increase during warmer periods and decrease during colder periods, while not covary with changes in the geomagnetic field intensity. To further distinguish the role of different paleoenvironmental factors, we compared magnetofossil abundance with planktonic δ18O, δ13C of organic matter, K/Al and Si/Al, which indicate continental ice volume (paleotemperature), organic matter origin, run‐off intensity and productivity, respectively. The results indicate that less continental ice volume (higher paleotemperature), enhanced productivity and run‐off intensity are closely related and jointly promoted magnetofossil production and preservation. Our study offers a comprehensive approach to understanding how magnetofossil assemblages relate to paleoenvironmental changes off the SW Iberian Margin.

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.

Biogeochemical Niche of Magnetotactic Cocci Capable of Sequestering Large Polyphosphate Inclusions in the Anoxic Layer of the Lake Pavin Water Column.

Magnetotactic bacteria (MTB) are microorganisms thriving mostly at oxic–anoxic boundaries of aquatic habitats. MTB are efficient in biomineralising or sequestering diverse elements intracellularly, which makes them potentially important actors in biogeochemical cycles. Lake Pavin is a unique aqueous system populated by a wide diversity of MTB with two communities harbouring the capability to sequester not only iron under the form of magnetosomes but also phosphorus and magnesium under the form of polyphosphates, or calcium carbonates, respectively. MTB thrive in the water column of Lake Pavin over a few metres along strong redox and chemical gradients representing a series of different microenvironments. In this study, we investigate the relative abundance and the vertical stratification of the diverse populations of MTB in relation to environmental parameters, by using a new method coupling a precise sampling for geochemical analyses, MTB morphotype description, and in situ measurement of the physicochemical parameters. We assess the ultrastructure of MTB as a function of depth using light and electron microscopy. We evidence the biogeochemical niche of magnetotactic cocci, capable of sequestering large PolyP inclusions below the oxic–anoxic transition zone. Our results suggest a tight link between the S and P metabolisms of these bacteria and pave the way to better understand the implication of MTB for the P cycle in stratified environmental conditions.

Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae.

Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (Fe3O4), and/or greigite (Fe3S4) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the Nitrospirae phylum can form up to several hundreds of Fe3O4 magnetosome crystals and dozens of sulfur globules in a single cell. These MTB are widespread in aquatic environments and sometimes account for a significant proportion of microbial biomass near the oxycline, linking these lineages to the key steps of global iron and sulfur cycling. Despite their ecological and biogeochemical importance, our understanding of the diversity and ecophysiology of magnetotactic Nitrospirae is still very limited because this group of MTB remains unculturable. Here, we identify and characterize two previously unknown MTB populations within the Nitrospirae phylum through a combination of 16S rRNA gene-based and genome-resolved metagenomic analyses. These two MTB populations represent distinct morphotypes (rod-shaped and coccoid, designated as XYR, and XYC, respectively), and both form more than 100 bullet-shaped magnetosomal crystals per cell. High-quality draft genomes of XYR and XYC have been reconstructed, and they represent a novel species and a novel genus, respectively, according to their average amino-acid identity values with respect to available genomes. Accordingly, the names Candidatus Magnetobacterium cryptolimnobacter and Candidatus Magnetomicrobium cryptolimnococcus for XYR and XYC, respectively, were proposed. Further comparative genomic analyses of XYR, XYC, and previously reported magnetotactic Nitrospirae reveal the general metabolic potential of this MTB group in distinct microenvironments, including CO2 fixation, dissimilatory sulfate reduction, sulfide oxidation, nitrogen fixation, or denitrification processes. A remarkably conserved magnetosome gene cluster has been identified across Nitrospirae MTB genomes, indicating its putative important adaptive roles in these bacteria. Taken together, the present study provides novel insights into the phylogenomic diversity and ecophysiology of this intriguing, yet poorly understood MTB group.

Mass collection of magnetotactic bacteria from the permanently stratified ferruginous Lake Pavin, France.

Obtaining high biomass yields of specific microorganisms for culture-independent approaches is a challenge faced by scientists studying organism's recalcitrant to laboratory conditions and culture. This difficulty is highly decreased when studying magnetotactic bacteria (MTB) since their unique behaviour allows their enrichment and purification from other microorganisms present in aquatic environments. Here, we use Lake Pavin, a permanently stratified lake in the French Massif Central, as a natural laboratory to optimize collection and concentration of MTB that thrive in the water column and sediments. A method is presented to separate MTB from highly abundant abiotic magnetic particles in the sediment of this crater lake. For the water column, different sampling approaches are compared such as in situ collection using a Niskin bottle and online pumping. By monitoring several physicochemical parameters of the water column, we identify the ecological niche where MTB live. Then, by focusing our sampling at the peak of MTB abundance, we show that the online pumping system is the most efficient for fast recovering of large volumes of water at a high spatial resolution, which is necessary considering the sharp physicochemical gradients observed in the water column. Taking advantage of aerotactic and magnetic MTB properties, we present an efficient method for MTB concentration from large volumes of water. Our methodology represents a first step for further multidisciplinary investigations of the diversity, metagenomic and ecology of MTB populations in Lake Pavin and elsewhere, as well as chemical and isotopic analyses of their magnetosomes.

Single-cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle.

Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that mineralize dissolved iron into intracellular magnetic crystals. After cell death, these crystals are trapped into sediments that remove iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits nitrogen fixation and primary productivity. A thorough assessment of their impact has been hampered by a lack of methodology to measure the amount of, and variability in, their intracellular iron content. We quantified the iron mass contained in single MTB cells of Magnetospirillum magneticum strain AMB-1 using a time-resolved inductively coupled plasma-mass spectrometry methodology. Bacterial iron content depends on the external iron concentration, and reaches a maximum value of ~10-6 ng of iron per cell. From these results, we calculated the flux of dissolved iron incorporation into environmental MTB populations and conclude that MTB may mineralize a significant fraction of dissolved iron into crystals.

Culture-independent characterization of a novel magnetotactic member affiliated to the Beta class of the Proteobacteria phylum from an acidic lagoon.

Magnetotactic bacteria (MTB) comprise a group of motile microorganisms common in most mesothermal aquatic habitats with pH values around neutrality. However, during the last two decades, a number of MTB from extreme environments have been characterized including: cultured alkaliphilic strains belonging to the Deltaproteobacteria class of the Proteobacteria phylum; uncultured moderately thermophilic strains belonging to the Nitrospirae phylum; cultured and uncultured moderately halophilic or strongly halotolerant bacteria affiliated with the Deltaproteobacteria and Gammaproteobacteria classes and an uncultured psychrophilic species belonging to the Alphaproteobacteria class. Here, we used culture-independent techniques to characterize MTB from an acidic freshwater lagoon in Brazil (pH ∼ 4.4). MTB morphotypes found in this acidic lagoon included cocci, rods, spirilla and vibrioid cells. Magnetite (Fe3 O4 ) was the only mineral identified in magnetosomes of these MTB while magnetite magnetosome crystal morphologies within the different MTB cells included cuboctahedral (present in spirilla), elongated prismatic (present in cocci and vibrios) and bullet-shaped (present in rod-shaped cells). Intracellular pH measurements using fluorescent dyes showed that the cytoplasmic pH was close to neutral in most MTB cells and acidic in some intracellular granules. Based on 16S rRNA gene phylogenetic analyses, some of the retrieved gene sequences belonged to the genus Herbaspirillum within the Betaproteobacteria class of the Proteobacteria phylum. Fluorescent in situ hybridization using a Herbaspirillum-specific probe hybridized with vibrioid MTB in magnetically-enriched samples. Transmission electron microscopy of the Herbaspirillum-like MTB revealed the presence of many intracellular granules and a single chain of elongated prismatic magnetite magnetosomes. Diverse populations of MTB have not seemed to have been described in detail in an acid environment. In addition, this is the first report of an MTB phylogenetically affiliated with Betaproteobacteria class.

Analysis of a population of magnetotactic bacteria of the Gulf of Gabès, Tunisia.

The occurrence of magnetotactic bacteria (MTB) on a Tunisian marine coast exposed to heavy metals pollution (Sfax, Gulf of Gabès, Mediterranean Sea) was investigated. The MTB population of this Southern Mediterranean coast was compared to the MTB populations previously investigated on the French Northern Mediterranean coast. A dominant MTB coccus morphotype was observed by microscopy analysis. By pyrosequencing technology, the analysis of the 16S ribosomal RNA (rDNA) revealed as much as 33 operational taxonomic sequence units (OTUs) close to sequences of MTB accessible in the databases. The majority were close to MTB sequences of the "Med group" of α-Proteobacteria. Among them, a dominant OTU_001 (99 % of the MTB sequences) affiliated within the Magnetococcales order was highlighted. Investigating the capacities of this novel bacterium to be used in bioremediation and/or depollution processes could be envisaged.

Magneto-chemotaxis in sediment: first insights.

Magnetotactic bacteria (MTB) use passive alignment with the Earth magnetic field as a mean to increase their navigation efficiency in horizontally stratified environments through what is known as magneto-aerotaxis (M-A). Current M-A models have been derived from MTB observations in aqueous environments, where a >80% alignment with inclined magnetic field lines produces a one-dimensional search for optimal living conditions. However, the mean magnetic alignment of MTB in their most widespread living environment, i.e. sediment, has been recently found to be <1%, greatly reducing or even eliminating the magnetotactic advantage deduced for the case of MTB in water. In order to understand the role of magnetotaxis for MTB populations living in sediment, we performed first M-A observations with lake sediment microcosms. Microcosm experiments were based on different combinations of (1) MTB position with respect to their preferred living depth (i.e. above, at, and below), and (2) magnetic field configurations (i.e. correctly and incorrectly polarized vertical fields, horizontal fields, and zero fields). Results suggest that polar magnetotaxis is more complex than implied by previous experiments, and revealed unexpected differences between two types of MTB living in the same sediment. Our main findings are: (1) all investigated MTB benefit of a clear magnetotactic advantage when they need to migrate over macroscopic distances for reaching their optimal living depth, (2) magnetotaxis is not used by all MTB under stationary, undisturbed conditions, (3) some MTB can rely only on chemotaxis for macroscopic vertical displacements in sediment while other cannot, and (4) some MTB use a fixed polar M-A mechanisms, while other can switch their M-A polarity, performing what can be considered as a mixed polar-axial M-A. These observations demonstrate that sedimentary M-A is controlled by complex mechanical, chemical, and temporal factors that are poorly reproduced in aqueous environments.

Magnetotaxis and acquisition of detrital remanent magnetization by magnetotactic bacteria in natural sediment: First experimental results and theory

The widespread occurrence of magnetotactic bacteria (MTB) in several types of marine and freshwater sediment, and the role of fossil magnetosomes (magnetofossils) as main remanent magnetization carriers therein, has important paleomagnetic and paleoenvironmental implications. Despite numerous studies on MTB biology and on magnetofossil preservation in geological records, no detailed information is yet available on how magnetotaxis (i.e., the ability to navigate along magnetic field lines) is performed in sedimentary environments, and on how magnetofossils possibly record the Earth magnetic field. We provide for the first time experimental evidence for these processes. MTB living in sediment are poorly aligned with the geomagnetic field, contrary to what is observed in water. This can explain the seemingly excessive magnetic moment of most MTB. The observed alignment is sufficient for supporting magnetotaxis across the typical thickness of chemical gradients. Experiments with magnetofossil‐rich sediment suggest that a natural remanent magnetization (NRM) is acquired by magnetofossils in the so‐called benthic mixed layer, where natural MTB populations usually occur. The acquired NRM is proportional to the applied field at least up to ∼160 µT, and its intensity is compatible with values observed in nature for same sediment types. Therefore, if fossil magnetosome chains are not subjected to further alteration by early diagenetic processes, they can provide useful relative paleointensities. We propose a preliminary model to explain early stages of magnetofossil NRM acquisition as the result of a dynamic equilibrium between magnetic torques and randomizing forces due to sediment mixing.

Single‐cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3

Magnetotactic bacteria (MTB) are a diverse group of prokaryotes that orient along magnetic fields using membrane-coated magnetic nanocrystals of magnetite (Fe(3) O(4) ) or greigite (Fe(3) S(4) ), the magnetosomes. Previous phylogenetic analysis of MTB has been limited to few cultivated species and most abundant members of natural populations, which were assigned to Proteobacteria and the Nitrospirae phyla. Here, we describe a single cell-based approach that allowed the targeted phylogenetic and ultrastructural analysis of the magnetotactic bacterium SKK-01, which was low abundant in sediments of Lake Chiemsee. Morphologically conspicuous single cells of SKK-01 were micromanipulated from magnetically collected multi-species MTB populations, which was followed by whole genome amplification and ultrastructural analysis of sorted cells. Besides intracellular sulphur inclusions, the large ovoid cells of SKK-01 harbour ∼175 bullet-shaped magnetosomes arranged in multiple chains that consist of magnetite as revealed by TEM and EDX analysis. Sequence analysis of 16 and 23S rRNA genes from amplified genomic DNA as well as fluorescence in situ hybridization assigned SKK-01 to the candidate division OP3, which so far lacks any cultivated representatives. SKK-01 represents the first morphotype that can be assigned to the OP3 group as well as the first magnetotactic member of the PVC superphylum.