Preface Magnetotactic Bacteria and Magnetoreception

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 4

Journal of Oceanology and Limnology

Vol. 39 No. 6, P. 2001-2004, 2021


https://doi.org/10.1007/s00343-021-2001-1

Preface
Magnetotactic bacteria and magnetoreception

Wei LIN1, 2, *, Long-Fei WU2, 3


1
Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing
100029, China
2
France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy
of Sciences, Beijing 100029, China
Aix Marseille Univ, CNRS, LCB, Centuri, IM2B, IMM, Marseille 13009, France
3

Received Jun. 6, 2021; accepted for publication Sep. 15, 2021


© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2021

A broad range of organisms have evolved abilities important roles of MTB in the global biogeochemical
to exploit the Earth’s magnetic field for orientation cycles in aquatic ecosystems (Lin et al., 2017; Amor
and navigation—a behavior known as et al., 2020). Biochemical and genetic studies using
magnetoreception (Nordmann et al., 2017). model MTB organisms including Magnetospirillum
Magnetotactic bacteria (MTB), diverse microbes magneticum strain AMB-1, M. gryphiswaldense
with a patchy distribution across the bacterial tree of strain MSR-1 and Desulfovibrio magneticus strain
life, are the best known and most extensively studied RS-1 have led to important advances in
magnetosensitive microorganisms. In order to understanding the underlying molecular mechanisms
efficiently achieve magnetotactic behavior, MTB of magnetosomal biosynthesis and magnetoreception
biomineralize intracellular chain-arranged magnetic (Uebe and Schüler, 2016; McCausland and Komeili,
single-domain crystals of magnetite (Fe3O4) and/or 2020). Collectively, MTB represent a unique model
greigite (Fe3S4) called magnetosomes, which are system for the study of intracellular
unique prokaryotic organelles that confer a magnetic biomineralization, prokaryotic organelle biogenesis,
moment to the cell and act as an internal compass and magnetoreception. For these reasons, MTB has
needle (Bazylinski and Frankel, 2004). become increasingly more attractive to researchers
Since the first discovery of MTB in the 1960s and from a variety of different disciplines.
1970s (Blakemore, 1975; Bellini, 2009; Frankel, This special issue “Magnetotactic Bacteria and
2009), the field has seen tremendous advances in Magnetoreception” brings together a series of 11
the diversity, ecology and ecophysiology of MTB, peer-reviewed research, opinion, and review articles
their magnetotactic behaviors, the magnetosome covering the breadth of research across MTB.
biomineralization mechanisms and the applications Understanding the magnetotactic behavior of MTB
of entire MTB cells and isolated magnetosomal and their diversity and distribution across different
nanoparticles. MTB have a worldwide distribution ecosystems is a crucial topic. Qian et al. (2021)
across marine, brackish and freshwater reveal that UV radiation in combination with
environments, although their occurrence in alternation of magnetic field direction in lab can
waterlogged soils has also been noted (Lin et al., trigger the reversal of magnetotactic swimming
2017). For many years, the known diversity of MTB direction, from north-seeking to south-seeking, and
was thought to fall into a few phyla (Amann et al., initiated the unidirectional division of a multicellular
2007; Kolinko et al., 2012); however, the magnetotactic prokaryote, which indicates a link
development of culture-independent techniques has between magnetic orientation of MTB and light.
recently revealed an unexpected phylogenetic However, understanding the reaction time scale and
diversity of MTB across the bacterial tree of life
(Lin et al., 2018, 2020; Uzun et al., 2020). Their
global distribution and high diversity imply * Corresponding author: weilin@mail.iggcas.ac.cn
2002 J. OCEANOL. LIMNOL., 39(6), 2021 Vol. 39

mechanism governing such behavior requires roles in making iron available for the local
integrated investigation. Chen et al. (2021b) examine microbial community and in the evolution of
the morphological and phylogenetic diversity of magnetosome biogenesis across different bacterial
MTB in a mangrove environment and demonstrate lineages, although further studies are required to
the existence of a highly diverse group of MTB in confirm this hypothesis.
this productive ecosystem at the transition between Three studies provide new insights into biology
terrestrial and marine environments. Cui et al. (2021) and magnetosomal biogenesis mechanisms of MTB.
extend the studies of MTB diversity and distribution This includes a review paper that summarizes recent
to the Caroline Seamount located in the south of the advances in redox modulation of magnetosome
Mariana Trench. Interestingly, the authors have biosynthesis in model Magnetospirillum strains (Li,
revealed the occurrence of abundant living MTB 2021). Through a combination of genetic approaches,
cells in sediments at water depths >1 500 m. This transmission electron microscopy observations and
finding, together with the previous studies (e.g., rock magnetic measurements, Wu et al. (2021)
Petermann and Bleil, 1993; Liu et al., 2017), identify an essential role of MamZ protein in
reinforces the widespread distribution of MTB in magnetosomal maturation process of
bathypelagic environments. MTB are generally M. gryphiswaldense strain MSR-1. They also note
considered as free-living microorganisms, but the close relationship between mamZ and other
recently several studies have revealed that MTB magnetosome genes located in mamXY operon
could live as symbionts of marine bivalves (Dufour during the maturation process of magnetosomal
et al., 2014) and protists (Monteil et al., 2019), crystals. Besides well-studied Magnetospirillum
which have a remarkable impact on our understanding strains, Du et al. (2021) report the genomic analysis
of MTB ecology and of magnetoreception evolution of a marine magnetotactic strain SH-1 belonging to
in other organisms. Metagenomic study considerably the genus Terasakiella that was recently isolated,
speeds up the progress of our understanding about which offers several insights into metabolism and
diversity, distribution, and ecological significance of magnetosomal biosynthesis in this novel MTB
MTB. A preliminary study in this issue by Simon et strain.
al. (2021) indicates that several bacterial species Both entire MTB cells and isolated magnetosome
closely related to known MTB exist in the human nanoparticles have great application potentials in
gut through a metagenomic analysis and these various fields of biotechnology and nanotechnology.
species appear to be related to magnetite-rich brain Two papers in this issue assess the potential
regions known to function in human orientation and applications of MTB cells. Chen et al. (2021a)
navigation. It should be noted that magnetosome- characterize the biocompatibility and safety of marine
associated genes are not found in these bacteria, thus magnetotactic bacteria strain MO-1. They argue that
further studies are necessary to confirm these cells of MO-1 could be potentially used in targeted
findings. How MTB are transmitted into human gut clinical therapy. The magnetic hyperthermia
and if they could maintain and reproduce there properties of M. gryphiswaldense strain MSR-1 have
remain open questions. been investigated by Zhang et al. (2021) using a
Two papers in this issue explore the ecology of combination of a commercial standard system and
MTB and their impacts on iron cycling. Chen et al. magnetic measurements. According to their findings,
(2021c) characterize a magnetically responsive cells of MSR-1 exhibit excellent magnetic
ciliate (tentatively identified as Uronemella hyperthermia ability and their heat generation
parafilificum HQ) collected from intertidal principle mainly follows the hysteresis loss
sediment of Huiquan Bay, Qingdao, China. The mechanism.
size and shape of magnetic particles within HQ are We are grateful to acknowledge the Editor-in-Chief
similar to those in MTB cells occurred in the same and editorial staff members of Journal of Oceanology
environment, which suggests that HQ has the and Limnology for giving opportunity for this special
ability to graze and digest MTB. This finding issue. We appreciate all the authors for their
highlights the potential function of HQ in the contributions and all the reviewers involved in
release of iron back into the ecosystem. Taveira et processing these articles. We hope that this issue will
al. (2021) in their opinion article propose that MTB be useful for researchers working on various aspects
infection by phages may play previously neglected related to MTB research.
No.6 LIN and WU: Magnetotactic bacteria and magnetoreception 2003

References magnetotactic bacterium within the candidate division


OP3. Environmental Microbiology, 14: 1709-1721,
Amann R, Peplies J, Schüler D. 2007. Diversity and https://doi.org/10.1007/s00343-009-0001-7.
taxonomy of magnetotactic bacteria. In: Schüler D ed. Li Y J. 2021. Redox control of magnetosome biomineralization.
Magnetoreception and Magnetosomes in Bacteria. Journal of Oceanology and Limnology, 39(6): 2070-2081,
Springer, Berlin. p.25-36. https://doi.org/10.1007/s00343-021-0397-2.
Amor M, Mathon F P, Monteil C L, Busigny V, Lefevre C T. Lin W, Pan Y, Bazylinski D A. 2017. Diversity and ecology of
2020. Iron-biomineralizing organelle in magnetotactic and biomineralization by magnetotactic bacteria.
bacteria: function, synthesis and preservation in ancient Environmental Microbiology Reports, 9(4): 345-356,
rock samples. Environmental Microbiology, 22(9): 3611- https://doi.org/10.1111/1758-2229.12550.
3632, https://doi.org/10.1111/1462-2920.15098. Lin W, Zhang W, Paterson G A, Zhu Q, Zhao X, Knight R,
Bazylinski D A, Frankel R B. 2004. Magnetosome formation Bazylinski D A, Roberts A P, Pan Y. 2020. Expanding
in prokaryotes. Nature Reviews: Microbiology, 2(3): 217- magnetic organelle biogenesis in the domain Bacteria.
230, https://doi.org/10.1038/nrmicro842. Microbiome, 8(1): 152, https://doi.org/10.1186/s40168-
Bellini S. 2009. On a unique behavior of freshwater bacteria. 020-00931-9.
Chinese Journal of Oceanology and Limnology, 27(3): Lin W, Zhang W, Zhao X, Roberts A P, Paterson G A,
3-5, https://doi.org/10.1007/s00343-009-0003-5. Bazylinski D A, Pan Y. 2018. Genomic expansion of
Blakemore R. 1975. Magnetotactic bacteria. Science, 190(4212): magnetotactic bacteria reveals an early common origin
377-379, https://doi.org/10.1126/science.170679. of magnetotaxis with lineage-specific evolution. The
Chen C Y, Wang P P, Wu L F, Song T. 2021a. Biocompatibility ISME Journal, 12(6): 1508-1519, https://doi.org/10.
of marine magnetotactic ovoid strain MO-1 for in vivo 1038/s41396-018-0098-9.
application. Journal of Oceanology and Limnology, Liu J, Zhang W, Li X, Li X, Chen X, Li J H, Teng Z, Xu C,
39(6): 2107-2115, https://doi.org/10.1007/s00343-021- Santini C L, Zhao L, Zhao Y, Zhang H, Zhang W J, Xu K,
0420-7. Li C, Pan Y, Xiao T, Pan H, Wu L F. 2017. Bacterial
Chen H T, Li J H, Wu L F, Zhang W J. 2021b. Morphological community structure and novel species of magnetotactic
and phylogenetic diversity of magnetotactic bacteria and bacteria in sediments from a seamount in the Mariana
multicellular magnetotactic prokaryotes from a mangrove volcanic arc. Scientific Reports, 7(1): 17964, https://doi.
ecosystem in the Sanya River, South China. Journal of org/10.1038/s41598-017-17445-4.
Oceanology and Limnology, 39(6): 2015-2026, https:// McCausland H C, Komeili A. 2020. Magnetic genes: studying
doi.org/10.1007/s00343-021-0491-5. the genetics of biomineralization in magnetotactic
Chen S, Cui K X, Zhang W Y, Zhao Y C, Xiao T, Pan H M, bacteria. PLoS Genetics, 16(2): e1008499, https://doi.
Zhang W C, Wu L F. 2021c. Observations on a org/10.1371/journal.pgen.1008499.
magnetotactic bacteria-grazing ciliate in sediment from Monteil C L, Vallenet D, Menguy N, Benzerara K, Barbe V,
the intertidal zone of Huiquan Bay, China. Journal of Fouteau S, Cruaud C, Floriani M, Viollier E, Adryanczyk
Oceanology and Limnology, 39(6): 2053-2062, https:// G, Leonhardt N, Faivre D, Pignol D, López-García P,
doi.org/10.1007/s00343-021-1011-3. Weld R J, Lefevre C T. 2019. Ectosymbiotic bacteria at
Cui K X, Zhang W Y, Liu J, Xu C, Zhao Y C, Chen S, Pan H the origin of magnetoreception in a marine protist. Nature
M, Xiao T, Wu L F. 2021. Characterization and diversity Microbiology, 4: 1088-1095, https://doi.org/10.1038/
of magnetotactic bacteria from sediments of Caroline s41564-019-0432-7.
Seamount in the Western Pacific Ocean. Journal of Nordmann G C, Hochstoeger T, Keays D A. 2017.
Oceanology and Limnology, 39(6): 2027-2043, https:// Magnetoreception—A sense without a receptor. PLoS
doi.org/10.1007/s00343-021-0029-x. Biology, 15(10): e2003234, https://doi.org/10.1371/
Du H J, Zhang W Y, Lin W, Pan H M, Xiao T, Wu L F. 2021. journal.pbio.2003234.
Genomic analysis of a pure culture of magnetotactic Petermann H, Bleil U. 1993. Detection of live magnetotactic
bacterium Terasakiella sp. SH-1. Journal of Oceanology bacteria in South-Atlantic deep-sea sediments. Earth and
and Limnology, 39(6): 2097-2106, https://doi. Planetary Science Letters, 117(1-2): 223-228, https://doi.
org/10.1007/s00343-021-1054-5. org/10.1016/0012-821X(93)90128-V.
Dufour S C, Laurich J R, Batstone R T, McCuaig B, Elliott A, Qian X X, Zhao Y C, Santini C L, Pan H M, Xiao T, Chen
Poduska K M. 2014. Magnetosome-containing bacteria H T, Song T, Li J H, Alberto F, Brustlein S, Wu L F.
living as symbionts of bivalves. The ISME Journal, 8(12): 2021. How light affect the magnetotactic behavior
2453-2462, https://doi.org/10.1038/ismej.2014.93. and reproduction of ellipsoidal multicellular
Frankel R B. 2009. The discovery of magnetotactic/ magnetoglobules? Journal of Oceanology and
magnetosensitive bacteria. Chinese Journal of Oceanology Limnology, 39(6): 2005-2014, https://doi.org/10.1007/
and Limnology, 27(3): 1-2, https://doi.org/10.1007/ s00343-021-0493-3.
s00343-009-0001-7. Simon R A, Ranasinghe P D, Barazanji N, Jungeström M
Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler B, Xu J, Bednarska O, Serrander L, Engström M,
D. 2012. Single-cell analysis reveals a novel uncultivated Bazylinski D A, Keita Å V, Walter S. 2021.
2004 J. OCEANOL. LIMNOL., 39(6), 2021 Vol. 39

Magnetotactic bacteria from the human gut microbiome 2020. Unravelling the diversity of magnetotactic bacteria
associated with orientation and navigation regions of through analysis of open genomic databases. Scientific
the brain. Journal of Oceanology and Limnology, Data, 7(1): 252, https://doi.org/10.1038/s41597-020-
39(6): 2044-2052, https://doi.org/10.1007/s00343- 00593-0.
021-0495-1. Wu S, Wang Q, Wang X, Guo R X, Zhang T W, Pan Y X, Li F,
Taveira I, Bazylinski D A, Abreu F. 2021. Release the iron: Li Y. 2021. MamZ protein plays an essential role in
does the infection of magnetotactic bacteria by phages magnetosome maturation process of Magnetospirillum
play a role in making iron available in aquatic gryphiswaldense MSR-1. Journal of Oceanology and
environments? Journal of Oceanology and Limnology, Limnology, 39(6): 2083-2097, https://doi.org/10.1007/
39(6): 2064-2070, https://doi.org/10.1007/s00343-021- s00343-021-0321-9.
1072-3. Zhang T W, Xu H T, Liu J, Pan Y X, Cao C Q. 2021.
Uebe R, Schüler D. 2016. Magnetosome biogenesis in Determination of the heating efficiency of magnetotactic
magnetotactic bacteria. Nature Reviews: Microbiology, bacteria in alternating magnetic field. Journal of
14(10): 621-637, https://doi.org/10.1038/nrmicro.2016.99. Oceanology and Limnology, 39(6): 2117-2127, https://
Uzun M, Alekseeva L, Krutkina M, Koziaeva V, Grouzdev D. doi.org/10.1007/s00343-021-1071-4.

You might also like