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

Teng, Zhao-Jie; Zhang, Yuyang; Zhang, Wenyan; Pan, Hongmiao; Xu, Jian-Hong; Huang, Hui; Xiao, Tian; Wu, Long-Fei

doi:10.3389/fmicb.2018.02135

Cited by 17 publications

(19 citation statements)

References 87 publications

(187 reference statements)

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“…This type of MMPs has been observed worldwide (Rodgers et al ., ; Simmons and Edwards, ; Winklhofer et al ., ; Wenter et al ., ; Shapiro et al ., ; Zhou et al ., ; Zhang et al ., ). Besides the spherical MMPs (sMMPs), we have identified another morphotype, the ellipsoidal or pineapple‐like MMPs (eMMPs) in the Mediterranean Sea (Lefèvre et al ., ; Chen et al ., ), the China Sea and the Pacific Ocean (Zhou et al ., ; Chen et al ., ; Du et al ., ; Dong et al ., ; Teng et al ., ). Approximately 60 cells aggregate into four to six interlacing circles to form a ~5–10 μM ellipsoidal entity.…”

Section: Introductionmentioning

confidence: 97%

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes

Qian

Santini

Kosta

et al. 2019

Environmental Microbiology

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Summary Multicellular magnetotactic prokaryotes (MMPs) exhibit peculiar coordination of swimming along geomagnetic field lines. Approximately 40–80 cells assemble, with a helical geometry or axisymmetry, into spherical or ellipsoidal MMPs respectively. To contribute to a comprehensive understanding of bacterial multicellularity here we took multiple microscopic approaches to study the diversity, assembly, reproduction and motility of ellipsoidal MMPs. Using correlative fluorescence in situ hybridization and scanning electron microscopy analysis, we found an unexpected diversity in populations of ellipsoidal MMPs in the Mediterranean Sea. The high‐pressure freezing/freeze substitution fixation technique allowed us to show, for the first time, that cells adhere via juxtaposed membranes and are held together by a rimming lattice. Fluorescence confocal microscopy and ultrathin section images revealed not only the one‐layer hollow three‐dimensional architecture, but also periphery–core unilateral constriction of constituent cells and unidirectional binary fission of the ellipsoidal MMPs. This finding suggests the evolution toward MMPs multicellularity via the mechanism of incomplete separation of offspring. Remarkably, thousands of flagellar at the periphery surface of cells underpin the coordinated swimming of MMPs in response to mechanical, chemical, magnetic and optical stimuli, including a magnetotactic photokinesis behaviour. Together these results unveil the unique structure and function property of ellipsoidal MMPs.

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Section: Introductionmentioning

confidence: 97%

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes

Qian

Santini

Kosta

et al. 2019

Environmental Microbiology

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“…The use of micromanipulation in studies involving genome sequences of MTB has been reported previously (Chen, et al 2015b, Jogler, et al 2011, Teng, et al 2018a, Teng, et al 2018b. WGA of the MTB was performed using the illustra Single Cell GenomiPhi DNA Amplification Kit (GE29-1080-39; Sigma, United States) following the manufacturer's instructions, with a 2.5-h amplification (Teng, et al 2018a, Teng, et al 2018b. PCR amplification (Mastercycler; Eppendorf, German) was conducted using the bacterial universal primers 27f and 1492r (Lane 1991) (Sangon Biotech, Shanghai, China).…”

Section: Phylogenetic Analysismentioning

confidence: 92%

“…For phylogenetic analysis of the MTB we combined micromanipulation with whole genome amplification (WGA) and polymerase chain reaction (PCR) amplification of the 16S rRNA gene. The use of micromanipulation in studies involving genome sequences of MTB has been reported previously (Chen, et al 2015b, Jogler, et al 2011, Teng, et al 2018a, Teng, et al 2018b. WGA of the MTB was performed using the illustra Single Cell GenomiPhi DNA Amplification Kit (GE29-1080-39; Sigma, United States) following the manufacturer's instructions, with a 2.5-h amplification (Teng, et al 2018a, Teng, et al 2018b.…”

Section: Phylogenetic Analysismentioning

confidence: 99%

“…Deltaproteobacterial MTB comprise a diverse and ecologically interactive group of sulfate-reducing bacteria (SRB). They have been found in various habitats including freshwater rivers, moats, lakes, and wetlands (Chen, et al 2013, Li, et al 2019, Sakaguchi, et al 1993; in brackish lagoons and springs (Lefèvre, et al 2011c, Lins andFarina 1999); marine intertidal zones, lagoons, and coral reefs (Chen, et al 2015b, Teng, et al 2018b; and in extreme hypersaline and highly alkaline environments (Lefèvre, et al 2011b, Martins, et al 2010. They include various morphological forms including unicells (Lefèvre, et al 2011c), chains of 25 cocci (barbells) (Simmons, et al 2006), and multicellular forms (multicellular magnetotactic prokaryotes: MMPs) (Delong, et al 1993, Zhou, et al 2013.…”

Section: Introductionmentioning

confidence: 99%

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

Pan

Dong

Teng

et al. 2019

FEMS Microbiology Letters

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Magnetotactic 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 brackish lagoon with algal bloom. Electron microscopy observations showed that they were ovoid to slightly curved rods having a mean length of 6.3 ± 1.1 μm and a mean width of 4.1 ± 0.4 μm. Each cell had a single polar flagellum. They contained hundreds of bullet-shaped intracellular magnetite magnetosomes. Phylogenetic analysis revealed that they were most closely related to Desulfamplus magnetovallimortis strain BW-1, and belonged to the Deltaproteobacteria. Our findings indicate that LR-1 may be a new species of MTB. We propose that deltaproteobacterial MTB may play an important role in iron cycling and so may represent a reservoir of iron, and be an indicator species for monitoring algal blooms in such eutrophic ecosystems. These observations provide new clues to the cultivation of magnetotactic Deltaproteobacteria and the control of algal blooms, although further studies are needed.

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“…Since then, these types of magnetoglobules have been observed worldwide [36][37][38][39][40][41][42]. The second morphotype, the ellipsoidal or pineapple-like magnetoglobules, were observed in the Mediterranean Sea [8,43,44], the China Sea, and the Pacific Ocean [45][46][47][48][49]. Approximately 60 cells axisymmetrically assemble along the longitudinal axis to achieve a one-layer hollow entity that is held by a lattice at the surface [8].…”

Section: Peritrichous Flagella Of Multicellular Magnetoglobulesmentioning

confidence: 99%

Flagella and Swimming Behavior of Marine Magnetotactic Bacteria

Zhang

2020

Biomolecules

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Marine environments are generally characterized by low bulk concentrations of nutrients that are susceptible to steady or intermittent motion driven by currents and local turbulence. Marine bacteria have therefore developed strategies, such as very fast-swimming and the exploitation of multiple directional sensing-response systems in order to efficiently migrate towards favorable places in nutrient gradients. The magnetotactic bacteria (MTB) even utilize Earth's magnetic field to facilitate downward swimming into the oxic-anoxic interface, which is the most favorable place for their persistence and proliferation, in chemically stratified sediments or water columns. To ensure the desired flagella-propelled motility, marine MTBs have evolved an exquisite flagellar apparatus, and an extremely high number (tens of thousands) of flagella can be found on a single entity, displaying a complex polar, axial, bounce, and photosensitive magnetotactic behavior. In this review, we describe gene clusters, the flagellar apparatus architecture, and the swimming behavior of marine unicellular and multicellular magnetotactic bacteria. The physiological significance and mechanisms that govern these motions are discussed.

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

Cited by 17 publications

References 87 publications

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes

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

Flagella and Swimming Behavior of Marine Magnetotactic Bacteria

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