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On the origin of microbial magnetoreception

  • Institute of Geology and Geophysics, Chinese Academy of Sciences

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A broad range of organisms, from prokaryotes to higher animals, have the ability to sense and utilize Earth's geomagnetic field—a behavior known as magnetoreception. Although our knowledge of the physiological mechanisms of magnetoreception has increased substantially over recent decades, the origin of this behavior remains a fundamental question in evolutionary biology. Despite this, there is growing evidence that magnetic iron mineral biosynthesis by prokaryotes may represent the earliest form of biogenic magnetic sensors on Earth. Here, we integrate new data from microbiology, geology and nanotechnology, and propose that initial biomineralization of intracellular iron nanoparticles in early life evolved as a mechanism for mitigating the toxicity of reactive oxygen species (ROS), as ultraviolet radiation and free-iron-generated ROS would have been a major environmental challenge for life on early Earth. This iron-based system could have later been co-opted as a magnetic sensor for magnetoreception in microorganisms, suggesting an origin of microbial magnetoreception as the result of the evolutionary process of exaptation.
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REVIEW National Science Review
7: 472–479, 2020
doi: 10.1093/nsr/nwz065
Advance access publication 21 May 2019
On the origin of microbial magnetoreception
Wei Lin1,2,3,, Joseph L. Kirschvink4,5, Greig A. Paterson1,6, Dennis A. Bazylinski7
and Yongxin Pan1,2,3,8,
1Key Laboratory of
Earth and Planetary
Physics, Institute of
Geology and
Geophysics, Chinese
Academy of Sciences,
Beijing 100029, China;
2Institutions of Earth
Science, Chinese
Academy of Sciences,
Beijing 100029, China;
3France-China Joint
Laboratory for
Evolution and
Development of
Organisms, Chinese
Academy of Sciences,
Beijing 100029, China;
4Division of
Geological &
Planetary Sciences,
California Institute of
Technology, Pasadena,
CA 91125, USA;
5Earth-Life Science
Institute, Tokyo
Institute of
Technology, Tokyo
152–8551, Japan;
6Department of Earth,
Ocean and Ecological
Sciences, University
of Liverpool, Liverpool,
L69 7ZE, UK; 7School
of Life Sciences,
University of Nevada
at Las Vegas, Las
Vegas, NV
89154-4004, USA and
8College of Earth and
Planetary Sciences,
University of Chinese
Academy of Sciences,
Beijing 100049, China
authors. E-mails:;
Received 7 March
2019; Revised 16
May 2019; Accepted
20 May 2019
A broad range of organisms, from prokaryotes to higher animals, have the ability to sense and utilize Earth’s
geomagnetic eld—a behavior known as magnetoreception. Although our knowledge of the physiological
mechanisms of magnetoreception has increased substantially over recent decades, the origin of this
behavior remains a fundamental question in evolutionary biology. Despite this, there is growing evidence
that magnetic iron mineral biosynthesis by prokaryotes may represent the earliest form of biogenic magnetic
sensors on Earth. Here, we integrate new data from microbiology, geology and nanotechnology, and
propose that initial biomineralization of intracellular iron nanoparticles in early life evolved as a mechanism
for mitigating the toxicity of reactive oxygen species (ROS), as ultraviolet radiation and free-iron-generated
ROS would have been a major environmental challenge for life on early Earth. is iron-based system could
have later been co-opted as a magnetic sensor for magnetoreception in microorganisms, suggesting an
origin of microbial magnetoreception as the result of the evolutionary process of exaptation.
Keywords: magnetoreception, biomineralization, magnetotactic bacteria, exaptation
Earth’s magnetosphere protects the surface environ-
ment from solar wind and cosmic radiation, and has,
therefore, been an essential factor in the persistence
of life on Earth. It has also provided a natural global
positioning system that various organisms have
exploited for navigation and migration via the genet-
ically controlled biomineralization of ferrimagnetic
iron minerals [1–3]. is iron-based magnetore-
ception has been identied in microorganisms
(prokaryotes and some protists) and diverse an-
imals from sh to mammals, suggesting that it
was a primal sensory system of all living systems
[4–12]. However, the origin and early evolution
of magnetoreception remain major enigmas. It has
been proposed that magnetoreception evolved from
a pre-existing trait (i.e. biomineralization) through
the process of exaptation [13], while, more recently,
a non-genetically controlled photoferrotrophy-
driven hypothesis has been proposed [14]. How
and why biogenic magnetic sensors rst evolved
remain maers of debate, and resolving these ques-
tions is important for understanding the origin and
evolution of magnetoreception not only in prokary-
otes, but also in eukaryotes. Here, we integrate new
data from microbiology, geology and nanotechnol-
ogy that support an exaptation model for microbial
magnetoreception (also known as magnetotaxis)
from an initial iron-based system for scavenging
intracellular free radicals generated by ultraviolet
radiation (UVR) and/or ferrous iron on early Earth.
One of the most extensively studied magnetic-
sensing organisms are magnetotactic bacteria
(MTB)—a group of diverse prokaryotes that
synthesize intracellular chain-arranged, nano-sized,
membrane-bounded magnetic crystals of mag-
netite (Fe3O4) and/or greigite (Fe3S4) called
magnetosomes [2]. Magnetosome chains are the
magnetic sensors in MTB, which act as an internal
compass needle and cause cells to align passively
along the local geomagnetic eld (Fig. 1). MTB
are the most primitive magnetic-sensing organisms
known thus far, with no current evidence of this
ability in viruses or the Archaea. In addition to
the MTB, magnetosome-like structures have been
e Author(s) 2019. Published by Oxford University Press on behalf of China Science Publishing & Media Ltd. is is an Open Access article distributed under the terms of the Creative
Commons Aribution License (hp://, which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original
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REVIEW Lin et al.473
Figure 1. A magnetotactic bacterium (2.2 μm in length) with a single chain of Fe3O4
magnetosomes (brown inclusions). A agellum is inserted schematically on the right
side of the cell. Magnetosomes impart a permanent magnetic dipole moment to the cell
and act as an internal compass needle, causing it to align passively along geomagnetic
eld lines as it swims.
discovered in eukaryotic algae, protozoans and
vertebrates [6,7], which led Vali and Kirschvink
[15] to propose that the rst eukaryotes may have
inherited the ability to biomineralize magnetosomes
from a magnetotactic alphaproteobacterium during
the endosymbiotic development of mitochondria,
with subsequent gene transfer to the nucleus.
MTB were discovered independently by Salva-
tore Bellini and Richard P. Blakemore in 1963 and
1974, respectively [4,16]. ese bacteria have a
global distribution in aquatic environments from
marine to freshwater ecosystems [17]. In addition,
they have been shown to be important in the global
biogeochemical cycling of Fe as well as other ele-
ments,suchasS,N,CandP[18–21]. In some envi-
ronments, magnetosomes from MTB are preserved
in sediments or rocks as fossils, referred to as mag-
netofossils [22,23]. Magnetofossils are important
contributions to the remanent magnetization of sed-
iments and have been suggested as biomarkers for
reconstructing paleoenvironmental conditions [24].
Magnetofossil records trace an evolutionary history
of MTB to the Cretaceous and, with less certainty, to
the Precambrian around 1.9 Ga [25].
Until a few years ago, all MTB were only as-
signed to one of two major bacterial phyla: the
Proteobacteria or the Nitrospirae [26]. Use of
cultivation-independent approaches (such as 16S
rRNA gene-targeting analyses, metagenomics and
single-cell genomics) has led to the discovery of
previously unidentied MTB lineages, which greatly
expands our knowledge of their diversity. MTB
have a patchy phylogenetic distribution and are
now known to lie within at least ve bacterial phyla,
including Proteobacteria,Nitrospirae,Planctomycetes
and the candidate phyla of Latescibacteria and
Omnitrophica, which suggests that the traits of
magnetotaxis and magnetosome biomineralization
occur widely in the domain Bacteria [17,27–29].
Molecular, genetic and genomic advances in
MTB have led to the identication of a large gene
cluster (referred to as a magnetosome gene clus-
ter or MGC) containing a group of genes involved
in magnetosome biomineralization and in construc-
tion of the magnetosome chain [30–35]. Because
of their essential roles in magnetotaxis, comparative
and phylogenetic analyses of MGCs from dierent
MTB taxonomies can shed light on the origin and
evolution of microbial magnetoreception in bacte-
ria. Recent expansion of MGCs has enabled the re-
construction of the evolutionary history of MTB,
which suggests a monophyletic origin of magne-
totaxis from a single common ancestor [33,36,37]
prior to or near the divergence between the Nitrospi-
rae and Proteobacteria phyla during the mid-Archean
Eon [38] or maybe even earlier, in the last com-
mon ancestor of the Proteobacteria,Nitrospirae,Om-
nitrophica,Latescibacteria and Planctomycetes phyla
(Fig. 2)[35]. Bacterial magnetotaxis, therefore, ap-
pears to be a primal physiological process and the
rst example of magnetoreception and the rst ex-
ample of controlled biomineralization on Earth.
Magnetotaxis is clearly the main function of magne-
tosomes in extant MTB. e presence of these iron
nanoparticles imparts a magnetic dipole moment on
MTB cells and enables the cells to orient passively,
which then allows them to swim actively along the
geomagnetic eld direction. In general, MTB also
appear to have a ‘polarity’—a preference to swim
in a particular direction under oxic conditions; that
is, they swim to the magnetic north in the north-
ern hemisphere and to the magnetic south in the
southern hemisphere [2], although several types of
MTB have the opposite polarity in each hemisphere
[39,40]. In conjunction with other tactic responses,
such as aerotaxis [41], phototaxis [42], chemotaxis
[43] or redox taxis [43], magnetotaxis allows MTB
to more eciently locate and maintain positions in
their preferred less-oxygenated microhabitats near
the oxic-anoxic transition zone in aquatic environ-
It has been estimated that, for a cell of a Mag-
netospirillum species, a magnetosome chain of 20
Fe3O4crystals would provide a sucient magnetic
dipole moment for magnetotaxis [44]. We note,
however, that as few as three to ve magnetosomes
per cell appear to be enough to provide a strong
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474 Natl Sci Rev, 2020, Vol. 7, No. 2 REVIEW
Evolutionary time Evolutionary time
Ancestral MTB
Magnetite magnetosome
Greigite magnetosome
Unknown type of magnetosome
MGC duplication and divergence
Horizontal gene transfers
Loss events of magnetite-type MGCs
Loss events of greigite-type MGCs
Ancestral MTB
Figure 2. Proposed scenarios for the evolution of magnetotaxis in bacteria at or above
the class or phylum taxonomic levels [35]. The last common ancestor of magnetotac-
tic bacteria (MTB) was either (a) magnetite-producing or (b) a bacterium containing an
unknown magnetosome type. Both scenarios suggest a monophyletic origin of mag-
netosome gene clusters (MGCs) from a single common ancestor that existed early in
Earth history. Vertical inheritance followed by multiple independent gene losses is a
major force that drove the evolution of magnetotaxis in bacteria at or above the class
or phylum levels [35,36], while, within lower-level ranks, the evolutionary history of
magnetotaxis appears to be much more complicated (e.g. [81–83]).
magnetic dipole for orientation in some uncultured
environmental MTB (Fig. 3). Some MTB, includ-
ing ‘Candidatus Magnetobacterium bavaricum’ [45]
and ‘Candidatus Magnetobacterium casensis’ [46]
from the Nitrospirae phylum, synthesize hundreds
of magnetosomes in a single cell—far greater than
would be needed for magnetotaxis. e redundancy
or ‘overproduction’ of magnetic particles suggests
that magnetosomes in MTB may have other func-
tions in addition to magnetotaxis.
Several possible functions have been suggested
for magnetosomes, such as iron storage and seques-
tration, electrochemical baeries, gravity sensors
or providing locally strong magnetic elds for
enhancing and stabilizing magnetochemical
reaction pathways involving free-radical pairs
[15,25,47,48]. All of these, however, await conr-
mation by experimental studies. Recently, however,
it has been shown experimentally that Fe3O4mag-
netosomes in some MTB exhibit peroxidase-like
activity that can eliminate intracellular levels of
reactive oxygen species (ROS) [49]. Moreover, this
activity can be further enhanced under irradiation
by visible light [50]. ese ndings indicate strongly
the potential functions of magnetosome nanoparti-
cles in the detoxication of ROS or toxic free iron.
Exaptation—an evolutionary process by which a
biological entity is co-opted for a new role that is
unrelated to its initial function [51]—was likely
central in the evolution of magnetotaxis. Accumu-
lating evidence indicates that microbial life was
present at least since the Archean [52–54] and,
as noted above, MTB appear to have originated
in the mid-Archean Eon [38]. During the early
to late Archean, the primordial atmosphere was
anoxic, with 105of the present atmospheric
level of molecular O2[55,56]. Due to the lack of
an eective ozone layer on early Earth, harmful
ultraviolet radiation (UVR) was considerably higher
than in the present day and would have exerted
signicant environmental selection pressure on
microorganisms in the surface and shallow-water
conditions [57]. High UVR levels are detrimental
to living microorganisms by either directly causing
lesions on native DNA molecules or indirectly
through the accumulation of ROS inside cells.
Archean oceans were predominantly anoxic, with
abundant dissolved ferrous iron (>30 μm) supplied
from mid-ocean ridges, hydrothermal vents and
500 nm 200 nm
3 magnetosomes 4 magnetosomes
200 nm
5 magnetosomes
Figure 3. Transmission electron microscope images of uncultured environmental magnetotactic bacteria with (a) three, (b)
four and (c) ve magnetosome particles per cell (white arrows point to each magnetosome), which indicates that three to
ve magnetosomes may provide a sufcient magnetic dipole moment for magnetotaxis in these bacteria.
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REVIEW Lin et al.475
Figure 4. Exaptation model of microbial magnetoreception on early Earth. (a) Reactive
oxygen species (ROS) were a major challenge to which ancient life had to adapt. ROS
would have been generated and enhanced through ultraviolet radiation (UVR) (yellow),
accumulating free Fe(II) inside cells (purple) and/or mineral-induced formation (orange).
(b) The ancestral role of intracellular iron-oxide nanoparticles (initial magnetosomes)
formed through ancient biomineralization processes was to help early life cope with
oxidative stress because of their antioxidant enzyme-like activities and reducing intra-
cellular free iron. (c) Initial magnetosomes were later co-opted to serve an additional
new role of magnetoreception as a mineral magnetic sensor. (d) Modication of mag-
netosomes by natural selection, such as the increase in magnetosome particles and
formation of a chain arrangement, would impart a greater magnetic dipole moment to
the cell, leading to much more efcient magnetotaxis.
sediment diagenesis [58]. Ferrous iron likely could
diuse passively through the outer membrane of pri-
mordial organisms and would have stimulated toxic
intracellular ROS levels through the Fenton reac-
tion [59]. Furthermore, ROS might have also been
present in aqueous, atmospheric and rock environ-
ments on early Earth because of the formation of rad-
ical species on mineral surfaces induced by UVR, im-
pact shocks and mechanical grinding [60,61]. ROS
accumulation could damage genetic material, dete-
riorate proteins, cause lipid peroxidation and disturb
cellular homeostasis [62]; therefore, dealing with
ROS was a major survival challenge for early life on
Earth (Fig. 4a).
Extant organisms have evolved various antioxi-
dant systems to detoxify ROS, such as superoxide
dismutases, peroxiredoxins and catalases in aerobes
and superoxide reductases in anaerobes and mi-
croaerophiles [63]. e appearance of appreciable
O2concentrations would have led to signicant
oxidative stress, so it is generally accepted that major
antioxidant defense systems evolved prior to the
Great Oxygenation Event (GOE), which marked
a permanent molecular O2rise in the atmosphere
between 2.4 and 2.1 billion years ago [64]. An-
tioxidant defense systems then radiated massively
aer the GOE [65]. It remains unclear whether life
evolved primordial antioxidant enzymes at or prior
to the mid-Archean Eon, although some studies
suggest that the last universal common ancestor
might have possessed pathways to remove ROS
Discovery of intrinsic peroxidase- and catalase-
like activities of iron-oxide nanoparticles (IONPs,
including Fe3O4)[67–69] and of peroxidase-like
properties of magnetosomes [49,50] leads us to
propose that some ancient life forms might have
relied on the intracellular biomineralization of
IONPs (initial magnetosomes) as antioxidants to
cope with ROS stress on early Earth. IONPs have
been found to have pH-dependent dual enzyme-like
activities in intracellular microenvironments—that
is, they catalyse H2O2to generate hydroxyl radicals
under acidic conditions through peroxidase-like
activities and catalyse H2O2to H2O and O2at
neutral and basic pH through catalase-like activities
[69]. e median pH of the cytoplasm, periplasm
and lumen of the magnetosome vesicle are generally
neutral in Magnetospirillum magneticum strain
AMB-1 cells [70], while the cytoplasmic pH of
some uncultured MTB from acidic environments
is also close to neutral [29], which indicates that
Fe3O4magnetosomes may also have catalase-like
activity in vivo. Compared to traditional antioxidant
enzymes, IONPs have enhanced enzyme-like stabil-
ity under extreme conditions such as a wide range
of temperatures (4–90C) and pH (1–12) [71],
which could enable them to maintain antioxidant
function in harsh environments.
Microorganisms on early Earth with the ability
to mitigate ROS stress would have a competitive
advantage. Here, we argue that iron nanoparticle
formation (initial magnetosomes) in early primal
life had the function of mitigating intracellular ROS
toxicity, through their intrinsic antioxidant enzyme-
like activities and reducing intracellular toxic free
iron (Fig. 4b). With increasing magnetosome num-
bers, it appears that magnetosomes were co-opted
to provide the cell with a magnetic dipole moment
for orientation along the geomagnetic eld—a for-
mation that was likely established 3–4 billion years
ago (Fig. 4c). is primal magnetosensitive struc-
ture, which reduces a 3D search to an optimized 1D
search along geomagnetic eld lines, appears to have
further protected ancient life from lethal UVR by
allowing ecient directed swimming to deeper wa-
ter with less O2at or near the oxic-anoxic transition
zone either in the water column, the sediment–water
interface or deeper in the sediment. For this to occur,
natural selection would favor the biomineralization
of high-coercivity single-domain magnetic nanopar-
ticles arranged as a chain with dipoles aligned in the
same direction to maximize the net magnetic dipole
moment for the individual cell to optimize magnetic
orientation and navigation (Fig. 4d).
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476 Natl Sci Rev, 2020, Vol. 7, No. 2 REVIEW
An interesting yet unanswered question is: what
was the mineral phase of the rst magnetic sensor?
According to our model, the rst magnetosomes
should have had antioxidant activities for scaveng-
ing intracellular ROS. A growing number of iron
nanoparticles, such as Fe3O4,Fe
2O3and FeS, have
been shown to exhibit enzyme-like activity [72]. It
has been suggested that Fe3O4might have been
the mineral present in the rst magnetosomes [37]
(Fig. 2a). Alternately, the last common ancestor
of MTB could have synthesized an unknown iron-
containing biomineral with enzyme-like activity that
later, during evolution, perhaps through intracellu-
lar changes in enzymatic activity or redox, resulted
in the generation of Fe3O4and Fe3S4particles [35]
(Fig. 2b). Identication of this rst mineral magnetic
sensor remains to be elucidated and is an area of ac-
tive investigation. e search for putative magneto-
fossils in older rocks and the reconstruction of ances-
tral MGC proteins both have the potential to answer
this question.
e exaptation model of magnetotaxis imposes
an expected evolutionary sequence of magnetosome
genes. at is, genes that are involved in magneto-
some biosynthesis should have originated earlier
than those for magnetosome positioning and crystal
size, and for the number of magnetosomes per cell.
Genetic studies of MGCs reveal eight (mamIELM-
NOBQ) and six (mamELMOQB) magnetosome
genes that are essential for Fe3O4magnetosome
biosynthesis in Magnetospirillum magneticum strain
AMB-1 and M.gryphiswaldense strain MSR-1, re-
spectively [31,73]. Homologues of these genes have
been identied in MGCs of other MTB, thereby
emphasizing their important roles in magnetosome
biomineralization. Additional genomic, phyloge-
netic and evolutionary analyses are clearly necessary
to investigate whether these essential genes evolved
earlier than those that control magnetosome chain
construction (e.g. mamK [74]ormamJ [75]),
magnetosome crystal size (mms6,mmsF,etc.
[31,73]) and the number of magnetosomes per
cell. Moreover, studies of the linear organization
of magnetosomes and formation of magnetosome
membrane vesicles may also shed light on the
evolution of the cytoskeleton and vacuole formation
in both prokaryotes and eukaryotes [15,76].
It is also clear that further research is required
to characterize systematically any additional mag-
netosome functions beside magnetotaxis in extant
MTB. For example, determining whether magne-
tosome crystals play a role in storing cellular iron,
or as an electrochemical baery or gravity sensor,
or for promoting magnetochemistry awaits further
study. We propose here that Fe3O4magnetosome
crystals act as a type of iron-oxide nanozyme [69,71]
in MTB with neutral intracellular pH by exhibit-
ing catalase-like activity in addition to peroxidase-
like activity, although further experimental evidence
is required to support this hypothesis. Lastly, why
some MTB biomineralize Fe3S4magnetosomes as
opposed to Fe3O4remains unclear, especially con-
sidering the generally less perfect chain alignment
and poorer crystallinity of Fe3S4magnetosomes
compared with those of Fe3O4magnetosomes [77].
Chemically synthesized Fe3S4nanoparticles have
also been shown to have peroxidase-like activ-
ity [78]. us, any further studies, such as those
noted above, should also include Fe3S4-producing
In space environments, UVR is one of the
most signicant hazards to living organisms. ere-
fore, the inferred adaptation of MTB to such
high-radiation environments makes them potential
model organisms in astrobiology research and may
provide an opportunity for studies on the responses
of organisms exposed to the near-space and low-
Earth-orbit space environments. Such studies could
in turn help to beer understand the origin and func-
tions of magnetosomes.
MTB are recognized as potentially signicant
contributors to present-day global iron cycling
[19,79]. Recent discovery of an Archean origin of
these magnetosensitive microorganisms further
suggests that they may have contributed to biogeo-
chemical cycling of iron throughout Earth’s history.
We suggest that the ROS-detoxication function
of magnetosomes and magnetotaxis capability
provided competitive advantages, which might
have helped ancient MTB to survive in diverse
aquatic environments on early Earth. Considering
their uptake of large amounts of environmental
iron and intracellular iron biomineralization, MTB
likely contributed to iron cycling on early Earth,
which further raises the question of whether these
microorganisms may have played as-yet-unknown
roles in the deposition of banded iron formations
that are distributed widely on the remnants of an-
cient cratons [80]. Future geochemical exploration
and magnetic characterization of both extant mag-
netosomes and magnetofossils will undoubtedly
provide new insights into this poorly understood,
yet geologically interesting, question.
e presence of precise biochemically controlled
biomineralization of ferrimagnetic minerals in two
domains of life provides strong evidence of Earth’s
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REVIEW Lin et al.477
magnetic biosphere. However, the initial origin and
subsequent evolutionary history of magnetorecep-
tion have not been investigated to any signicant
degree. We posit that ancient magnetoreception in
prokaryotes might have originated via an exaptation
process from pre-existing intracellular iron nanopar-
ticles that initially decreased the toxicity of ROS in
early life forms. us, magnetosome particles in an-
cient life served a detoxication role and were later
co-opted for microbial magnetoreception or magne-
totaxis. is exaptation origin of magnetotaxis pro-
vides a conceptual model for study of the origin
and evolution of magnetoreception, as well as poten-
tially providing a genetic template for other biomin-
eralization systems and mechanisms. With the ever-
increasing genomic data from both cultivated and
uncultivated MTB as well as advancement of molec-
ular, genetic, chemical and evolutionary technolo-
gies, we anticipate great progress in understand-
ing microbial magnetoreception in the near future.
Shedding further light on the evolutionary origin of
this system will also provide additional constraints
on the paleoenvironments under which it evolved as
well as on the development of magnetoreception in
higher organisms.
W.L. and Y.P. acknowledge nancial support from the Strate-
gic Priority Research Program of Chinese Academy of Sciences
(XDA17010501) and the National Natural Science Foundation
of China (NSFC) (41621004). W.L. acknowledges support from
the NSFC (41822704) and the Youth Innovation Promotion
Association of the Chinese Academy of Sciences. J.L.K. is sup-
ported by the US National Aeronautics and Space Administra-
tion Exobiology (EXO14 2-0176). G.A.P. acknowledges sup-
port from the NSFC (41574063) and the Natural Environment
Research Council (NERC) Independent Research Fellowship
(NE/P017266/1). D.A.B. is supported by the US National Sci-
ence Foundation (NSF) (EAR-1423939).
1. Kirschvink JL, Walker MM and Diebel CE. Magnetite-based
magnetoreception. Curr Opin Neurobiol 2001; 11: 462–7.
2. Bazylinski DA and Frankel RB. Magnetosome formation in
prokaryotes. Nat Rev Microbiol 2004; 2: 217–30.
3. Shaw J, Boyd A and House M et al. Magnetic particle-mediated
magnetoreception. J R Soc Interface 2015; 12: 499.
4. Blakemore RP. Magnetotactic bacteria. Science 1975; 190: 377–
5. Walker MM, Kirschvink JL and Chang S-BR et al. A candidate
magnetic sense organ in the yellown tuna, Thunnus albacares.
Science 1984; 224: 751–3.
6. Dearaujo FFT, Pires MA and Frankel RB et al. Magnetite and
magnetotaxis in algae. Biophys J 1986; 50: 375–8.
7. Mann S, Sparks NHC and Walker MM et al. Ultrastructure, mor-
phology and organization of biogenic magnetite from sockeye
salmon, Oncorhynchus nerka: implications for magnetorecep-
tion. JExpBiol1988; 140: 35–49.
8. Tian L, Xiao B and Lin W et al. Testing for the presence of
magnetite in the upper-beak skin of homing pigeons. Biometals
2007; 20: 197–203.
9. Bauer GB, Fuller M and Perry A et al. Magnetoreception and
biomineralization of magnetite in Cetaceans. In: Kirschvink JL,
Jones DS and MacFadden BJ (eds). Magnetite Biomineraliza-
tion and Magnetoreception in Organisms: a New Biomagnetism.
Boston: Springer US, 1985, 489–507.
10. Bazylinski DA, Lef `
evre CT and Frankel RB et al. Magnetotactic
protists at the oxic-anoxic transition zones of coastal aquatic
environments. In: Altenbach AV, Bernhard JM and Seckbach J
(eds). Anoxia,Vol.21. Dordrecht: Springer Netherlands, 2012,
11. Holland RA, Kirschvink JL and Doak TG et al. Bats use mag-
netite to detect the earth’s magnetic eld. PLoS One 2008; 3:
12. Tian L, Lin W and Zhang S et al. Bat head contains soft magnetic
particles: evidence from magnetism. Bioelectromagnetics 2010;
31: 499–503.
13. Kirschvink JL and Hagadorn JW. A grand unied theory of
biomineralization. In: B¨
auerlein E (ed). The Biomineralisation
of Nano- and Micro-Structures. Weinheim: Wiley-VCH Verlag
GmbH, 2000, 139–50.
14. Strbak O and Dobrota D. Archean iron-based metabolism anal-
ysis and the photoferrotrophy-driven hypothesis of microbial
magnetotaxis origin. Geomicrobiol J 2019; 36: 278–90.
15. Vali H and Kirschvink JL. Observations of magnetosome orga-
nization, surface structure, and iron biomineralization of unde-
scribed magnetotactic bacteria: evolutionary speculations. In:
Frankel RB and Blakemore RP (eds). Iron Biominerals. New York:
Plenum Press, 1990, 278–90.
16. Bellini S. On a unique behavior of freshwater bacteria. Chin J
Ocean Limnol 2009; 27:35.
17. Lin W, Pan Y and Bazylinski DA. Diversity and ecology of and
biomineralization by magnetotactic bacteria. Env Microbiol Rep
2017; 9: 345–56.
18. Cox BL, Popa R and Bazylinski DA et al. Organization and ele-
mental analysis of P-, S-, and Fe-rich inclusions in a population
of freshwater magnetococci. Geomicrobiol J 2002; 19: 387–406.
19. Lin W, Bazylinski DA and Xiao T et al. Life with compass: diver-
sity and biogeography of magnetotactic bacteria. Environ Micro-
biol 2014; 16: 2646–58.
20. Rivas-Lamelo S, Benzerara K and Lef`
evre CT et al. Magnetotac-
tic bacteria as a new model for P sequestration in the ferrugi-
nous Lake Pavin. Geochem Persp Let 2017: 35–41.
21. Schulz-Vogt HN, Pollehne F and J ¨
urgens K et al. Effect of large
magnetotactic bacteria with polyphosphate inclusions on the
phosphate prole of the suboxic zone in the Black Sea. ISME
J2019; 13 : 1198–208.
22. Chang SBR and Kirschvink JL. Magnetofossils, the magnetiza-
tion of sediments, and the evolution of magnetite biomineral-
ization. Annu Rev Earth Planet Sci 1989; 17: 169–95.
Downloaded from by California Institute of Technology user on 28 May 2020
478 Natl Sci Rev, 2020, Vol. 7, No. 2 REVIEW
23. Vasiliev I, Franke C and Meeldijk JD et al. Putative greigite magnetofossils from
the Pliocene epoch. Nat Geosci 2008; 1: 782–6.
24. Pan YX, Deng CL and Liu QS et al. Biomineralization and magnetism of bacterial
magnetosomes. Chin Sci Bull 2004; 49: 2563–8.
25. Kopp RE and Kirschvink JL. The identication and biogeochemical interpreta-
tion of fossil magnetotactic bacteria. Earth-Sci Rev 2008; 86: 42–61.
26. Jogler C and Sch¨
uler D. Genomics, genetics, and cell biology of magnetosome
formation. Annu Rev Microbiol 2009; 63: 501–21.
27. Kolinko S, Jogler C and Katzmann E et al. Single-cell analysis reveals a novel
uncultivated magnetotactic bacterium within the candidate division OP3. Env-
iron Microbiol 2012; 14: 1709–21.
28. Lin W and Pan Y. A putative greigite type magnetosome gene cluster from
the candidate phylum Latescibacteria. Env Microbiol Rep 2015; 7: 237–
29. Abreu F, Le ˜
ao P and Vargas G et al. Culture-independent characterization of a
novel uncultivated magnetotactic member of the Betaproteobacteria class of
the Proteobacteria phylum from an acidic lagoon. Environ Microbiol 2018; 20:
30. Gr¨
unberg K, Wawer C and Tebo BM et al. A large gene cluster encoding sev-
eral magnetosome proteins is conserved in different species of magnetotactic
bacteria. Appl Environ Microb 2001; 67: 4573–82.
31. Murat D, Quinlan A and Vali H et al. Comprehensive genetic dissection of the
magnetosome gene island reveals the step-wise assembly of a prokaryotic or-
ganelle. Proc Natl Acad Sci USA 2010; 107: 5593–8.
32. Lohße A, Ullrich S and Katzmann E et al. Functional analysis of the magneto-
some island in Magnetospirillum gryphiswaldense: the mamAB operon is suf-
cient for magnetite biomineralization. PLoS One 2011; 6: e25561.
33. Abreu F, Cantao ME and Nicolas MF et al. Common ancestry of iron oxide- and
iron-sulde-based biomineralization in magnetotactic bacteria. ISME J 2011;
5: 1634–40.
34. Lef`
evre CT, Trubitsyn D and Abreu F et al. Comparative genomic analysis of
magnetotactic bacteria from the Deltaproteobacteria provides new insights
into magnetite and greigite magnetosome genes required for magnetotaxis.
Environ Microbiol 2013; 15: 2712–35.
35. Lin W, Zhang W and Zhao X et al. Genomic expansion of magnetotactic bacte-
ria reveals an early common origin of magnetotaxis with lineage-specic evo-
lution. ISME J 2018; 12: 1508–19.
36. Lef`
evre CT and Bazylinski DA. Ecology, diversity, and evolution of magnetotactic
bacteria. Microbiol Mol Biol R 2013; 77: 497–526.
37. Lef`
evre CT, Trubitsyn D and Abreu F et al. Monophyletic origin of magnetotaxis
and the rst magnetosomes. Environ Microbiol 2013; 15: 2267–74.
38. Lin W, Paterson GA and Zhu Q et al. Origin of microbial biomineralization and
magnetotaxis during the Archean. Proc Natl Acad Sci USA 2017; 114: 2171–
39. Simmons SL, Bazylinski DA and Edwards KJ. South-seeking magnetotactic bac-
teria in the Northern Hemisphere. Science 2006; 311: 371–4.
40. Le˜
ao P, Teixeira LCRS and Cypriano J et al. North-seeking magnetotactic
Gammaproteobacteria in the Southern Hemisphere. Appl Environ Microbiol
2016; 82: 5595–602.
41. Frankel RB, Bazylinski DA and Johnson MS et al. Magneto-aerotaxis in marine
coccoid bacteria. Biophys J 1997; 73: 994–1000.
42. Shapiro OH, Hatzenpichler R and Buckley DH et al. Multicellular photo-
magnetotactic bacteria. Environ Microbiol Rep 2011; 3: 233–8.
43. Spring S and Bazylinski DA. Magnetotactic bacteria. In: Dworkin M (ed). The
Prokaryotes: An Evolving Electronic Resource for the Microbiological Commu-
nity. New York: Springer Verlag, 2006, 842–62.
44. Frankel RB, Zhang J-P and Bazylinski DA. Single magnetic domains in magne-
totactic bacteria. J Geophys Res 1998; 103: 30601–4.
45. Spring S, Amann R and Ludwig W et al. Dominating role of an unusual mag-
netotactic bacterium in the microaerobic zone of a freshwater sediment. Appl
Environ Microbiol 1993; 59: 2397–403.
46. Lin W, Deng A and Wang Z et al. Genomic insights into the uncultured genus
‘Candidatus Magnetobacterium’ in the phylum Nitrospirae. ISME J 2014; 8:
47. Kirschvink JL. Rock magnetism linked to human brain magnetite. Eos TransAGU
1994; 75: 178–9.
48. Uebe R and Sch¨
uler D. Magnetosome biogenesis in magnetotactic bacteria.
Nat Rev Microbiol 2016; 14: 621–37.
49. Guo FF, Yang W and Jiang W et al. Magnetosomes eliminate intracellular re-
active oxygen species in Magnetospirillum gryphiswaldense MSR-1. Environ
Microbiol 2012; 14: 1722–9.
50. Li K, Wang P and Chen C et al. Light irradiation helps magnetotactic bacte-
ria eliminate intracellular reactive oxygen species. Environ Microbiol 2017; 19:
51. Gould SJ and Vrba ES. Exaptation—a missing term in the science of form.
Paleobiology 1982; 8: 4–15.
52. Allwood AC, Walter MR and Burch IW et al. 3.43 billion-year-old stromatolite
reef from the Pilbara Craton of Western Australia: ecosystem-scale insights to
early life on Earth. Precambrian Res 2007; 158: 198–227.
53. Allwood AC, Grotzinger JP and Knoll AH et al. Controls on development and
diversity of Early Archean stromatolites. Proc Natl Acad Sci USA 2009; 106:
54. Sugitani K, Lepot K and Nagaoka T et al. Biogenicity of morphologically diverse
carbonaceous microstructures from the ca. 3400 Ma Strelley pool formation, in
the Pilbara Craton, Western Australia. Astrobiology 2010; 10: 899–920.
55. Poulton SW and Caneld DE. Ferruginous conditions: a dominant feature of the
ocean through Earth’s history. Elements 2011; 7: 107–12.
56. Johnson JE, Gerpheide A and Lamb MP et al. O2constraints from Paleopro-
terozoic detrital pyrite and uraninite. Geol Soc Am Bull 2014; 126: 813–30.
57. Cnossen I, Sanz-Forcada J and Favata F et al. Habitat of early life: Solar X-
ray and UV radiation at Earth’s surface 4–3.5 billion years ago. J Geophys Res
2007; 112: E02008.
58. Kendall B, Anbar AD and Kappler A et al. The global iron cycle. In: Knoll AH,
Caneld DE and Konhauser KO (eds). Fundamentals of Geobiology West Sus-
sex : John Wiley & Sons, Ltd, 2012, 65–92.
59. Winterbourn CC. Toxicity of iron and hydrogen peroxide: the Fenton reaction.
Toxicol Lett 1995; 82–83: 969–74.
60. Schoonen M, Smirnov A and Cohn C. A perspective on the role of minerals in
prebiotic synthesis. AMBIO: A Journal of the Human Environment 2004; 33:
61. Xu J, Sahai N and Eggleston CM et al. Reactive oxygen species at the
oxide/water interface: formation mechanisms and implications for prebiotic
chemistry and the origin of life. Earth Planet Sci Lett 2013; 363: 156–67.
62. TouatiD. Iron and oxidative stress in bacteria. Arch Biochem Biophys 2000; 373:
63. ´
Slesak I, ´
Slesak H and Zimak-Piekarczyk P et al. Enzymatic antioxidant systems
in early anaerobes: theoretical considerations. Astrobiology 2016; 16: 348–58.
64. Lyons TW, Reinhard CT and Planavsky NJ. The rise of oxygen in Earth’s early
ocean and atmosphere. Nature 2014; 506: 307–15.
65. Kirschvink JL, Gaidos EJ and Bertani LE et al. Paleoproterozoic snowball Earth:
extreme climatic and geochemical global change and its biological conse-
quences. Proc Natl Acad Sci USA 2000; 97: 1400–5.
Downloaded from by California Institute of Technology user on 28 May 2020
REVIEW Lin et al.479
66. ´
Slesak I, ´
Slesak H and Kruk J. Oxygen and hydrogen peroxide in the early evo-
lution of life on Earth: in silico comparative analysis of biochemical pathways.
Astrobiology 2012; 12: 775–84.
67. Gao L, Zhuang J and Nie L et al. Intrinsic peroxidase-like activity of ferromag-
netic nanoparticles. Nat Nanotech 2007; 2: 577–83.
68. Ragg R, Tahir MN and Tremel W. Solids go bio: inorganic nanoparticles as en-
zyme mimics. Eur J Inorg Chem 2016; 2016: 1906–15.
69. Chen Z, Yin J-J and Zhou Y-T et al. Dual enzyme-like activities of iron ox-
ide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano
2012; 6: 4001–12.
70. Eguchi Y, Fukumori Y and Taoka A. Measuring magnetosomal pH of the mag-
netotactic bacterium Magnetospirillum magneticum AMB-1 using pH-sensitive
uorescent proteins. Biosci Biotechnol Biochem 2018; 8451:19.
71. Gao L, Fan K and Yan X. Iron oxide nanozyme: a multifunctional enzyme mimetic
for biomedical applications. Theranostics 2017; 7: 3207–27.
72. Wei H and Wang E. Nanomaterials with enzyme-like characteristics
(nanozymes): next-generation articial enzymes. Chem Soc Rev 2013; 42:
73. Lohße A, Borg S and Raschdorf O et al. Genetic dissection of the mamAB
and mms6 operons reveals a gene set essential for magnetosome biogen-
esis in Magnetospirillum gryphiswaldense. J Bacteriol 2014; 196: 2658–
74. Komeili A, Li Z and Newman DK et al. Magnetosomes are cell membrane
invaginations organized by the actin-like protein MamK. Science 2006; 311:
75. Scheffel A, Gruska M and Faivre D et al. An acidic protein aligns magneto-
somes along a lamentous structure in magnetotactic bacteria. Nature 2006;
440: 110–4.
76. Grant CR, Wan J and Komeili A. Organelle formation in Bacteria and Archaea.
Annu Rev Cell Dev Biol 2018; 34: 217–38.
77. P´
osfai M, Buseck PR and Bazylinski DA et al. Iron suldes from magnetotactic
bacteria; structure, composition, and phase transitions. Am Mineral 1998; 83:
78. Ding C, Yan Y and Xiang D et al. Magnetic Fe3S4 nanoparticles with
peroxidase-like activity, and their use in a photometric enzymatic glucose as-
say. Microchim Acta 2016; 183: 625–31.
79. Chen AP, Berounsky VM and Chan MK et al. Magnetic properties of unculti-
vated magnetotactic bacteria and their contribution to a stratied estuary iron
cycle. Nat Commun 2014; 5: 4797.
80. Frankel RB. Fossil record: magnetic skeletons in Davy Jones’ locker. Nature
1986; 320: 575.
81. Rioux J-B, Philippe N and Pereira S et al. A second actin-like MamK protein in
Magnetospirillum magneticum AMB-1 encoded outside the genomic magneto-
some island. PLoS One 2010; 5: e9151.
82. Ji B, Zhang SD and Zhang WJ et al. The chimeric nature of the
genomes of marine magnetotactic coccoid-ovoid bacteria denes a
novel group of Proteobacteria. Environ Microbiol 2017; 19: 1103–19.
83. Monteil CL, Perri `
ere G and Menguy N et al. Genomic study of a novel magne-
totactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis.
Environ Microbiol 2018; 20: 4415–30.
Downloaded from by California Institute of Technology user on 28 May 2020
... As the first type of magnetosensitive and biomineralizing organisms, MTB are proposed to co-evolve with the hostile radiative subaerial environments on the Archean Earth possibly through exaptation, which shifted the function of magnetosome formation from either iron storage [31] or detoxification to magnetotaxis [32]. With magnetosomes, MTB were able to not only scavenge their intracellular free radicals but also guide themselves away from shallow to deeper subaqueous oxic-anoxic interface zones where neither radiation doses nor destructive oxygen species were plentiful [32,33]. ...
... As the first type of magnetosensitive and biomineralizing organisms, MTB are proposed to co-evolve with the hostile radiative subaerial environments on the Archean Earth possibly through exaptation, which shifted the function of magnetosome formation from either iron storage [31] or detoxification to magnetotaxis [32]. With magnetosomes, MTB were able to not only scavenge their intracellular free radicals but also guide themselves away from shallow to deeper subaqueous oxic-anoxic interface zones where neither radiation doses nor destructive oxygen species were plentiful [32,33]. Due to the similarity of early Mars to early Earth, the emergence of MTB-like life on Mars is an intriguing possibility and of course needs more investigation (Fig. 1D). ...
Full-text available
Capable of forming magnetofossils similar to some magnetite nanocrystals observed in the Martian meteorite ALH84001, magnetotactic bacteria (MTB) once occupied a special position in the field of astrobiology during the 1990s and 2000s. This flourish of interest in putative Martian magnetofossils faded from all but the experts studying magnetosome formation, based on claims that abiotic processes could produce magnetosome-like magnetite crystals. Recently, the rapid growth in our knowledge of the extreme environments in which MTB thrive and their phylogenic heritage, leads us to advocate for a renaissance of MTB in astrobiology. In recent decades, magnetotactic members have been discovered alive in natural extreme environments with wide ranges of salinity (up to 90 g L-1), pH (1-10), and temperature (0-70 °C). Additionally, some MTB populations are found to be able to survive irradiated, desiccated, metal-rich, hypomagnetic, or microgravity conditions, and are capable of utilizing simple inorganic compounds such as sulfate and nitrate. Moreover, MTB likely emerged quite early in Earth's history, coinciding with a period when the Martian surface was covered with liquid water as well as a strong magnetic field. MTB are commonly discovered in suboxic or oxic-anoxic interfaces in aquatic environments or sediments similar to ancient crater lakes on Mars, such as Gale crater and Jezero crater. Taken together, MTB can be exemplary model microorganisms in astrobiology research, and putative ancient Martian life, if it ever occurred, could plausibly have included magnetotactic microorganisms. Furthermore, we summarize multiple typical biosignatures that can be applied for the detection of ancient MTB on Earth and extraterrestrial MTB-like life. We suggest transporting MTB to space stations and simulation chambers to further investigate their tolerance potential and distinctive biosignatures to aid in understanding the evolutionary history of MTB and the potential of magnetofossils as an extraterrestrial biomarker.
... For example, diatoms can use silicate in the environment to form a finely structured silica shell on the cell surface, which can provide them with mechanical protection, photonic crystals and pH buffers [16,17]. In addition, there are some bacteria that can use internal magnetite crystals (Fe 3 O 4 or Fe 3 S 4 ) as magnetic sensors [13,18]. Inspired by the natural biomineralization phenomenon, artificial cell-material hybrid has received increasing interest for green chemistry and engineered living biomaterials [19,20]. ...
Full-text available
Photosynthetic energy conversion for high-energy chemicals generation is one of the most viable solutions to the quest for sustainable energy towards carbon neutrality. Microalgae are fascinating photosynthetic organisms, which can directly convert solar energy to chemical energy and electrical energy. However, microalgal photosynthetic energy has not yet been applicated at large scale, due to the limitation of their own characteristics. Researchers have been inspired to couple microalgae with synthetic materials via biomimetic assembly, and the resulting microalgae-material hybrids become more robust and even perform new functions. In the past decade, great progress has been made in microalgae-material hybrid, such as photosynthetic carbon dioxide fixation, photosynthetic hydrogen production, photoelectrochemical energy conversion, and even biochemical energy conversion for biomedical therapy. Microalgae-material hybrid offers opportunities to promote artificially enhanced photosynthesis research and synchronously inspires investigation of biotic-abiotic interface manipulation. This review summarizes current construction methods of microalgae-material hybrids and highlights their implication in energy and health. Moreover, we discuss the current problems and future challenges for microalgae-material hybrids and the outlook for their development and applications. This review will provide inspiration for rational design of microalgae-based semi-natural biohybrid and further promote the disciplinary fusion of material science and biological science.
... This sense is extremely important for explaining the phenomenon of bionavigation. Magnetoreception has been observed in bacteria [Lin et al., 2020], invertebrates (bees [Hsu and Weng, 2021], fruit fl ies [Gegear et al., 2008], butterfl ies [Dreyer et al., 2018], ants [Fleischmann et al., 2018]), and vertebrates (birds [Wiltschko and Wiltschko, 2019], turtles [Harrison et al., 2021], cartilaginous fi sh [Newton and Kajiura, 2017], bony fi sh [Scanlan et al., 2018], anurans [Shakhparonov and Ogurtsov, 2017], rodents [Malewski et al., 2018], and bats [Lindecke et al., 2021]). ...
Full-text available
The continuously changing magnetic fi eld of the Earth and its constant infl uence on the vital activity of all living organisms makes studies of magnetobiological effects important and in demand. The effects of weak magnetic fi elds, especially weak static magnetic fi elds, on living objects remains inappropriately understudied. The biological effects of weak magnetic fi elds result from chemical processes involving radicals, radical ions, and paramagnetic particles. As attenuation of the magnetic fi eld is a stress factor for the body and given that the nervous system performs the most important regulatory functions in forming the body’s stress response, this review addresses the infl uences of weak static magnetic fi elds on the functioning of the nervous system. Our own and published data are summarized; these indicate that weak static magnetic fi elds affect key biological processes, such as gene expression, cell proliferation and differentiation, and apoptosis, as well as behavior. Special attention is paid to the therapeutic potential of weak magnetic fi elds for clinical use in neurological pathologies
... The so-called "magnetoreception"-that is, spatial orientation by terrestrial magnetism-is a subject of scientific investigation [48] and controversy. Some experts on the subject have suggested that the formation of magnetite nanoparticles may have occurred before the emergence of eukaryotic cells [49]. The results obtained here indicated that magnetic particles occur as very small particles, at the nanometer scale. ...
Full-text available
Magnetite (Fe3O4) nanoparticles were extracted from the shells of freshwater Limnoperna fortunei (Dunker 1857) and marine Perna perna (Linnaeus 1758) mussels, followed by full physical and chemical characterization using ICP-OES, UV–Vis, EDX, Raman, and XRD spectroscopy, VSM magnetometry, and SEM and TEM techniques. Considering their spatial distribution, the ferrimagnetic particles in the shells had low concentration and presented superparamagnetic behavior characteristics of materials of nanometric size. Transmission electron microscopy (TEM, especially HRTEM) indicated round magnetic particles around 100 nm in size, which were found to be aggregates of nanoparticles about 5 nm in size. The TEM data indicated no iron oxide particles at the periostracum layer. Nevertheless, roughly round iron (hydr)oxide nanoparticle aggregates were found in the nacre, namely, the aragonite layer. As the aragonite layer is responsible for more than 97% of the shell of L. fortunei and considering the estimated size of the magnetic nanoparticles, we infer that these particles may be distributed homogeneously throughout the shell.
... as intracellular sensors that are thought to direct the aerotactic swimming motility along vertical redox gradients in the aquatic sediments, where MTB occur abundantly and ubiquitously (1)(2)(3). In the well-studied alphaproteobacterium Magnetospirillum gryphiswaldense (MSR-1) and closely related MTB, biosynthesis of magnetosomes has recently been demonstrated to be a rather intricate step-wise process, which is initiated by the formation of magnetosome vesicles by invagination from the cytoplasmic membrane (CM). ...
Full-text available
Magnetosomes of magnetotactic bacteria (MTB) consist of structurally perfect, nano-sized magnetic crystals enclosed within vesicles of a proteo-lipid membrane. In species of Magnetospirillum, biosynthesis of their cubo-octahedral-shaped magnetosomes was recently demonstrated to be a complex process, governed by about 30 specific genes that are comprised within compact magnetosome gene clusters (MGCs). Similar, yet distinct gene clusters were also identified in diverse MTB that biomineralize magnetosome crystals with different, genetically encoded morphologies. However, since most representatives of these groups are inaccessible by genetic and biochemical approaches, their analysis will require the functional expression of magnetosome genes in foreign hosts. Here, we studied whether conserved essential magnetosome genes from closely and remotely related MTB can be functionally expressed by rescue of their respective mutants in the tractable model Magnetospirillum gryphiswaldense of the Alphaproteobacteria . Upon chromosomal integration, single orthologues from other magnetotactic Alphaproteobacteria restored magnetosome biosynthesis to different degrees, while orthologues from distantly related Magnetococcia and Deltaproteobacteria were found to be expressed but failed to re-induce magnetosome biosynthesis, possibly due to poor interaction with their cognate partners within multiprotein magnetosome organelle of the host. Indeed, co-expression of the known interactors MamB and MamM from the alphaproteobacterium Magnetovibrio blakemorei increased functional complementation. Furthermore, a compact and portable version of the entire MGCs of M. magneticum was assembled by transformation-associated recombination cloning, and it restored the ability to biomineralize magnetite both in deletion mutants of the native donor and M. gryphiswaldense , while co-expression of gene clusters from both M. gryphiswaldense and M. magneticum resulted in overproduction of magnetosomes. IMPORTANCE We provide proof of principle that Magnetospirillum gryphiswaldense is a suitable surrogate host for the functional expression of foreign magnetosome genes and extended the transformation-associated recombination cloning platform for the assembly of entire large magnetosome gene cluster, which could then be transplanted to different magnetotactic bacteria. The reconstruction, transfer, and analysis of gene sets or entire magnetosome clusters will be also promising for engineering the biomineralization of magnetite crystals with different morphologies that would be valuable for biotechnical applications.
... By using the geomagnetic field as a source of spatial information, many organisms, from magnetotactic bacteria (MTB) to plants and animals, could better adapt to environmental and climate changes. Examples include long-distance animal migration/navigation and up-and-down MTB magnetotaxis shuttle [8,9]. We recently found that mice experiencing long-term exposure to hypomagnetic fields exhibit significant impairments of adult hippocampal neurogenesis and hippocampus-dependent learning, implying that the geomagnetic field is essential for mammals [10]. ...
Full-text available
This perspective argues an evolutionary effect of geomagnetic field reversals on life and highlights the urgency of multidisciplinary studies on the linkage between Earth's magnetic field and biosphere.
Some organisms have the unique capacity to geolocate and navigate in response to the Earth’s magnetic field lines. Migratory birds and fishes are the best-documented animals that evolved this capacity to guide their movements. In the microbial world, magnetotactic bacteria (MTB) and multicellular magnetotactic prokaryotes (MMPs) have been the only known magnetoreceptive microorganisms for decades. Some microeukaryotes also orient their motility axis along magnetic field lines thanks to the exploitation of MTB magnetism. The magnetic guidance of these prokaryotes and eukaryotes is due to the biomineralization of magnetic crystals. This article provides a brief overview of the current knowledge concerning the different multicellular prokaryotes and micro/macroeukaryotes capable of magnetoreception. We also discuss the evolution of this unique ability.
Magnetofossils are magnetic nanoparticles that represent the fossil remains of microorganisms that biomineralize magnetic minerals in a genetically controlled manner. Most magnetofossils found in the geologic record are produced by magnetotactic bacteria, which use them for navigating within their living environment. Magnetofossils can be identified using a combination of magnetic and imaging techniques. A common attribute of magnetofossils, although not pervasive, is that they are arranged in chains, which determines their specific magnetic properties. Magnetofossil signatures have been reported from ancient rocks to modern sediments and even in extraterrestrial materials. They provide a window into biomineralization, past environments, and ancient magnetic fields, as well as supplying fuel for questions on the origin of life in the Solar System.
Full-text available
Photosynthetic energy conversion for high-energy chemicals generation is one of the most viable solutions in the quest for sustainable energy towards carbon neutrality. Microalgae are fascinating photosynthetic organisms, which can directly convert solar energy into chemical energy and electrical energy. However, microalgal photosynthetic energy has not yet been applied on a large scale due to the limitation of their own characteristics. Researchers have been inspired to couple microalgae with synthetic materials via biomimetic assembly and the resulting microalgae–material hybrids have become more robust and even perform new functions. In the past decade, great progress has been made in microalgae–material hybrids, such as photosynthetic carbon dioxide fixation, photosynthetic hydrogen production, photoelectrochemical energy conversion and even biochemical energy conversion for biomedical therapy. The microalgae–material hybrid offers opportunities to promote artificially enhanced photosynthesis research and synchronously inspires investigation of biotic–abiotic interface manipulation. This review summarizes current construction methods of microalgae–material hybrids and highlights their implication in energy and health. Moreover, we discuss the current problems and future challenges for microalgae–material hybrids and the outlook for their development and applications. This review will provide inspiration for the rational design of the microalgae-based semi-natural biohybrid and further promote the disciplinary fusion of material science and biological science.
Full-text available
Nanozymes are nanomaterials with enzyme-like characteristics (Chem. Soc. Rev., 2013, 42, 6060-6093). They have been developed to address the limitations of natural enzymes and conventional artificial enzymes. Along with the significant advances in nanotechnology, biotechnology, catalysis science, and computational design, great progress has been achieved in the field of nanozymes since the publication of the above-mentioned comprehensive review in 2013. To highlight these achievements, this review first discusses the types of nanozymes and their representative nanomaterials, together with the corresponding catalytic mechanisms whenever available. Then, it summarizes various strategies for modulating the activity and selectivity of nanozymes. After that, the broad applications from biomedical analysis and imaging to theranostics and environmental protection are covered. Finally, the current challenges faced by nanozymes are outlined and the future directions for advancing nanozyme research are suggested. The current review can help researchers know well the current status of nanozymes and may catalyze breakthroughs in this field.
Full-text available
The origin and evolution of magnetoreception, which in diverse prokaryotes and protozoa is known as magnetotaxis and enables these microorganisms to detect Earth's magnetic field for orientation and navigation, is not well understood in evolutionary biology. The only known prokaryotes capable of sensing the geomagnetic field are magnetotactic bacteria (MTB), motile microorganisms that biomineralize intracellular, membrane-bounded magnetic single-domain crystals of either magnetite (Fe3O4) or greigite (Fe3S4) called magnetosomes. Magnetosomes are responsible for magnetotaxis in MTB. Here we report the first large-scale metagenomic survey of MTB from both northern and southern hemispheres combined with 28 genomes from uncultivated MTB. These genomes expand greatly the coverage of MTB in the Proteobacteria, Nitrospirae, and Omnitrophica phyla, and provide the first genomic evidence of MTB belonging to the Zetaproteobacteria and "Candidatus Lambdaproteobacteria" classes. The gene content and organization of magnetosome gene clusters, which are physically grouped genes that encode proteins for magnetosome biosynthesis and organization, are more conserved within phylogenetically similar groups than between different taxonomic lineages. Moreover, the phylogenies of core magnetosome proteins form monophyletic clades. Together, these results suggest a common ancient origin of iron-based (Fe3O4and Fe3S4) magnetotaxis in the domain Bacteria that underwent lineage-specific evolution, shedding new light on the origin and evolution of biomineralization and magnetotaxis, and expanding significantly the phylogenomic representation of MTB.
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Iron oxide nanoparticles have been widely used in many important fields due to their excellent nanoscale physical properties, such as magnetism/superparamagnetism. They are usually assumed to be biologically inert in biomedical applications. However, iron oxide nanoparticles were recently found to also possess intrinsic enzyme-like activities, and are now regarded as novel enzyme mimetics. A special term, "Nanozyme", has thus been coined to highlight the intrinsic enzymatic properties of such nanomaterials. Since then, iron oxide nanoparticles have been used as nanozymes to facilitate biomedical applications. In this review, we will introduce the enzymatic features of iron oxide nanozyme (IONzyme), and summarize its novel applications in biomedicine.
Despite its biological and geological significance, the origin of microbial magnetosome biomineralization, as well as the evolution of magnetotaxis, is still not well understood. Recently, the origin of magnetotaxis has been proposed to already exist in the Archean Eon. However, the Archean environment was fully anoxic. Therefore, what was the reason for the evolution of magnetotaxis in the anoxic Archean ocean and what mechanism could lead to the formation of single domain-sized magnetite nanoparticles that are a necessary condition of magnetotaxis functionality? Since the genetically controlled magnetosomes formation is extremely energetically demanding, in this review, we analyze Archean anoxic iron-based metabolism and we delineate the alternative possibilities of non-genetically controlled magnetosomes precursor origin as a necessary condition of magnetotaxis emergence. We show that coupling of anoxygenic photosynthesis with ferrous iron as an electron donor, with anaerobic respiration with ferric iron as an electron acceptor, provided sufficient material for non-genetically controlled magnetite formation. The co-evolution of cyanobacteria is suggested as the possible environmental pressure responsible for the emergence of Archean magnetotaxis. In accordance with the hypothesis of the reactive oxygen species-protective function of the first magnetosomes, we show that the formation of single domain-sized magnetite nanoparticles did not have to be initially connected with magnetotaxis origin, neither had to be genetically controlled nor intracellular. Instead, it could result from the long-lasting ambient pressure of metabolically produced extracellular iron oxide minerals in photoferrotrophs together with the emergence of local oxygen oases. The presence of oxygen could favor cells with the ability to navigate into oxic-anoxic transition zones since the oxygen was entirely toxic to Archean life. This evolutionary advantageous trait could finally result in a niche construction origin of genes responsible for intracellular magnetosome formation, which have remained preserved until today.
The Black Sea is the world’s largest anoxic basin and a model system for studying processes across redox gradients. In between the oxic surface and the deeper sulfidic waters there is an unusually broad layer of 10–40 m, where neither oxygen nor sulfide are detectable. In this suboxic zone, dissolved phosphate profiles display a pronounced minimum at the upper and a maximum at the lower boundary, with a peak of particulate phosphorus in between, which was suggested to be caused by the sorption of phosphate on sinking particles of metal oxides. Here we show that bacterial polyphosphate inclusions within large magnetotactic bacteria related to the genus Magnetococcus contribute substantially to the observed phosphorus peak, as they contain 26–34% phosphorus compared to only 1–5% in metal-rich particles. Furthermore, we found increased gene expression for polyphosphate kinases by several groups of bacteria including Magnetococcaceae at the phosphate maximum, indicating active bacterial polyphosphate degradation. We propose that large magnetotactic bacteria shuttle up and down within the suboxic zone, scavenging phosphate at the upper and releasing it at the lower boundary. In contrast to a passive transport via metal oxides, this bacterial transport can quantitatively explain the observed phosphate profiles.
Uncovering the mechanisms that underlie the biogenesis and maintenance of eukaryotic organelles is a vibrant and essential area of biological research. In comparison, little attention has been paid to the process of compartmentalization in bacteria and archaea. This lack of attention is in part due to the common misconception that organelles are a unique evolutionary invention of the "complex" eukaryotic cell and are absent from the "primitive" bacterial and archaeal cells. Comparisons across the tree of life are further complicated by the nebulous criteria used to designate subcellular structures as organelles. Here, with the aid of a unified definition of a membrane-bounded organelle, we present some of the recent findings in the study of lipid-bounded organelles in bacteria and archaea. Expected final online publication date for the Annual Review of Cell and Developmental Biology Volume 34 is October 6, 2018. Please see for revised estimates.
Ecological and evolutionary processes involved in magnetotactic bacteria (MTB) adaptation to their environment have been a matter of debate for many years. Ongoing efforts for their characterization are progressively contributing to understand these processes, including the genetic and molecular mechanisms responsible for biomineralization. Despite numerous culture‐independent MTB characterizations, essentially within the Proteobacteria phylum, only few species have been isolated in culture because of their complex growth conditions. Here, we report a newly cultivated magnetotactic, microaerophilic and chemoorganoheterotrophic bacterium isolated from the Mediterranean Sea in Marseille, France: Candidatus Terasakiella magnetica strain PR‐1 that belongs to an Alphaproteobacteria genus with no magnetotactic relative. By comparing the morphology and the whole genome shotgun sequence of this MTB with those of closer relatives, we brought further evidence that the apparent vertical ancestry of magnetosome genes suggested by previous studies within Alphaproteobacteria hides a more complex evolutionary history involving horizontal gene transfers and/or duplication events before and after the emergence of Magnetospirillum, Magnetovibrio and Magnetospira genera. A genome‐scale comparative genomics analysis identified several additional candidate functions and genes that could be specifically associated to MTB lifestyle in this class of bacteria. This article is protected by copyright. All rights reserved.
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 Delta‐ 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 (Fe3O4) 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. This article is protected by copyright. All rights reserved.
Magnetotactic bacteria synthesize uniform-sized and regularly shaped magnetic nanoparticles in their organelles termed magnetosomes. Homeostasis of the magnetosome lumen must be maintained for its role accomplishment. Here, we developed a method to estimate the pH of a single living cell of the magnetotactic bacterium Magnetospirillum magneticum AMB-1 using a pH-sensitive fluorescent protein E²GFP. Using the pH measurement, we estimated that the cytoplasmic pH was approximately 7.6 and periplasmic pH was approximately 7.2. Moreover, we estimated pH in the magnetosome lumen and cytoplasmic surface using fusion proteins of E²GFP and magnetosome-associated proteins. The pH in the magnetosome lumen increased during the exponential growth phase when magnetotactic bacteria actively synthesize magnetite crystals, whereas pH at the magnetosome surface was not affected by the growth stage. This live-cell pH measurement method will help for understanding magnetosome pH homeostasis to reveal molecular mechanisms of magnetite biomineralization in the bacterial organelle.
The role of microorganisms in the geochemical cycle of P has received great interest in the context of enhanced biological phosphorus removal and phosphorite formation. Here, we combine scanning and transmission electron microscopies, confocal laser scanning microscopy and synchrotron-based x-ray microfluorescence to analyse the distribution of P at the oxic-anoxic interface in the water column of the ferruginous Lake Pavin. We show that magnetotactic bacteria of the Magnetococcaceae family strongly accumulate polyphosphates and appear as P hotspots in the particulate fraction at this depth. This high accumulation may be characteristic of this family and may also relate to the chemical conditions prevailing in the lake. As a result, these magnetotactic cocci can be considered as new models playing a potentially important role in the P geochemical cycle, similar to sulphide oxidising bacteria such as Thiomargarita and Beggiatoa but thriving in a ferruginous, poorly sulphidic environment.