Restoration and Modification of Magnetosome Biosynthesis by Internal Gene Acquisition in a Magnetotactic Bacterium
Abstract
We report that the Integration of a large-sized DNA fragment into a chromosome is an important strategy for characterization of cellular functions in microorganisms. Magnetotactic bacteria synthesize intracellular organelles comprising membrane-bound single crystalline magnetite, also referred to as magnetosomes. Magnetosomes have gained interest in both scientific and engineering sectors as they can be utilized as a material for biomedical and nanotechnological applications. Although genetic engineering of magnetosome biosynthesis mechanism has been investigated, the current method requires cumbersome gene preparation processes. Here, the chromosomal integration of a plasmid containing ≈27 magnetosome genes (≈26 kbp region) in a non-magnetic mutant of Magnetospirillum magneticum AMB-1 using a broad-host-range plasmid is shown. The genome sequencing of gene-complemented strains reveals the chromosomal integration of the plasmid with magnetosome genes at a specific site, most likely by catalysis of an endogenous transposase. Magnetosome production is successfully enhanced by integrating a variation of magnetosome gene operons in the chromosome. This chromosomal integration mechanism will allow the design of functional magnetosomes de novo and M. magneticum AMB-1 may be used as a chassis for the designed magnetosome production.
- Authors:
-
- Tokyo Univ. of Agriculture and Technology (Japan)
- Tokyo Institute of Technology (Japan)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Tokyo Univ. of Agriculture and Technology (Japan); Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka (Japan)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Japan Society for the Promotion of Science (JSPS)
- OSTI Identifier:
- 1845297
- Grant/Contract Number:
- AC02-05CH11231; 16H02421; 18H01794
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biotechnology Journal
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 12; Journal ID: ISSN 1860-6768
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; magnetotactic bacteria; genetic engineering; chromosomal integration; biomineralization; bioproduction
Citation Formats
Arakaki, Atsushi, Goto, Mayu, Maruyama, Mina, Yoda, Takuto, Tanaka, Masayoshi, Yamagishi, Ayana, Yoshikuni, Yasuo, and Matsunaga, Tadashi. Restoration and Modification of Magnetosome Biosynthesis by Internal Gene Acquisition in a Magnetotactic Bacterium. United States: N. p., 2020.
Web. doi:10.1002/biot.202000278.
Arakaki, Atsushi, Goto, Mayu, Maruyama, Mina, Yoda, Takuto, Tanaka, Masayoshi, Yamagishi, Ayana, Yoshikuni, Yasuo, & Matsunaga, Tadashi. Restoration and Modification of Magnetosome Biosynthesis by Internal Gene Acquisition in a Magnetotactic Bacterium. United States. https://doi.org/10.1002/biot.202000278
Arakaki, Atsushi, Goto, Mayu, Maruyama, Mina, Yoda, Takuto, Tanaka, Masayoshi, Yamagishi, Ayana, Yoshikuni, Yasuo, and Matsunaga, Tadashi. Wed .
"Restoration and Modification of Magnetosome Biosynthesis by Internal Gene Acquisition in a Magnetotactic Bacterium". United States. https://doi.org/10.1002/biot.202000278. https://www.osti.gov/servlets/purl/1845297.
@article{osti_1845297,
title = {Restoration and Modification of Magnetosome Biosynthesis by Internal Gene Acquisition in a Magnetotactic Bacterium},
author = {Arakaki, Atsushi and Goto, Mayu and Maruyama, Mina and Yoda, Takuto and Tanaka, Masayoshi and Yamagishi, Ayana and Yoshikuni, Yasuo and Matsunaga, Tadashi},
abstractNote = {We report that the Integration of a large-sized DNA fragment into a chromosome is an important strategy for characterization of cellular functions in microorganisms. Magnetotactic bacteria synthesize intracellular organelles comprising membrane-bound single crystalline magnetite, also referred to as magnetosomes. Magnetosomes have gained interest in both scientific and engineering sectors as they can be utilized as a material for biomedical and nanotechnological applications. Although genetic engineering of magnetosome biosynthesis mechanism has been investigated, the current method requires cumbersome gene preparation processes. Here, the chromosomal integration of a plasmid containing ≈27 magnetosome genes (≈26 kbp region) in a non-magnetic mutant of Magnetospirillum magneticum AMB-1 using a broad-host-range plasmid is shown. The genome sequencing of gene-complemented strains reveals the chromosomal integration of the plasmid with magnetosome genes at a specific site, most likely by catalysis of an endogenous transposase. Magnetosome production is successfully enhanced by integrating a variation of magnetosome gene operons in the chromosome. This chromosomal integration mechanism will allow the design of functional magnetosomes de novo and M. magneticum AMB-1 may be used as a chassis for the designed magnetosome production.},
doi = {10.1002/biot.202000278},
journal = {Biotechnology Journal},
number = 12,
volume = 15,
place = {United States},
year = {Wed Aug 26 00:00:00 EDT 2020},
month = {Wed Aug 26 00:00:00 EDT 2020}
}
Works referenced in this record:
Conjugative and mobilizable genomic islands in bacteria: evolution and diversity
journal, July 2014
- Bellanger, Xavier; Payot, Sophie; Leblond-Bourget, Nathalie
- FEMS Microbiology Reviews, Vol. 38, Issue 4
A Hypervariable 130-Kilobase Genomic Region of Magnetospirillum gryphiswaldense Comprises a Magnetosome Island Which Undergoes Frequent Rearrangements during Stationary Growth
journal, November 2005
- Ullrich, Susanne; Kube, Michael; Schübbe, Sabrina
- Journal of Bacteriology, Vol. 187, Issue 21
A Novel Protein Tightly Bound to Bacterial Magnetic Particles in Magnetospirillum magneticum Strain AMB-1
journal, December 2002
- Arakaki, Atsushi; Webb, John; Matsunaga, Tadashi
- Journal of Biological Chemistry, Vol. 278, Issue 10
Biochemical and Proteomic Analysis of the Magnetosome Membrane in Magnetospirillum gryphiswaldense
journal, February 2004
- Grunberg, K.; Muller, E. -C.; Otto, A.
- Applied and Environmental Microbiology, Vol. 70, Issue 2
Iron feeding optimization and plasmid stability in production of recombinant bacterial magnetic particles by Magnetospirillum magneticum AMB-1 in fed-batch culture
journal, January 2001
- Yang, Chendong; Takeyama, Haruko; Matsunaga, Tadashi
- Journal of Bioscience and Bioengineering, Vol. 91, Issue 2
Structural insight into magnetochrome-mediated magnetite biomineralization
journal, October 2013
- Siponen, Marina I.; Legrand, Pierre; Widdrat, Marc
- Nature, Vol. 502, Issue 7473
The magnetosome membrane protein, MmsF, is a major regulator of magnetite biomineralization in Magnetospirillum magneticum AMB-1: MmsF is a regulator of magnetite biomineralization
journal, July 2012
- Murat, Dorothée; Falahati, Veesta; Bertinetti, Luca
- Molecular Microbiology, Vol. 85, Issue 4
Gene transfer in magnetic bacteria: transposon mutagenesis and cloning of genomic DNA fragments required for magnetosome synthesis
journal, May 1992
- Matsunaga, T.; Nakamura, C.; Burgess, J. G.
- Journal of Bacteriology, Vol. 174, Issue 9
The cation diffusion facilitator proteins MamB and MamM of Magnetospirillum gryphiswaldense have distinct and complex functions, and are involved in magnetite biomineralization and magnetosome membrane assembly: Functions of MamB and MamM in M. gryphiswaldense
journal, October 2011
- Uebe, René; Junge, Katja; Henn, Verena
- Molecular Microbiology, Vol. 82, Issue 4
Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria
journal, August 2009
- Nakazawa, H.; Arakaki, A.; Narita-Yamada, S.
- Genome Research, Vol. 19, Issue 10
Tn7 elements: Engendering diversity from chromosomes to episomes
journal, January 2009
- Parks, Adam R.; Peters, Joseph E.
- Plasmid, Vol. 61, Issue 1
Co-ordinated functions of Mms proteins define the surface structure of cubo-octahedral magnetite crystals in magnetotactic bacteria: Mms proteins define surface structure of magnetite
journal, July 2014
- Arakaki, Atsushi; Yamagishi, Ayana; Fukuyo, Ayumi
- Molecular Microbiology, Vol. 93, Issue 3
Magnetite formation by a magnetic bacterium capable of growing aerobically
journal, August 1991
- Matsunaga, Tadashi; Sakaguchi, Toshifumi; Tadakoro, Fumihiko
- Applied Microbiology and Biotechnology, Vol. 35, Issue 5
Formation of magnetite by bacteria and its application
journal, June 2008
- Arakaki, Atsushi; Nakazawa, Hidekazu; Nemoto, Michiko
- Journal of The Royal Society Interface, Vol. 5, Issue 26
Comparative analysis of magnetosome gene clusters in magnetotactic bacteria provides further evidence for horizontal gene transfer
journal, May 2009
- Jogler, Christian; Kube, Michael; Schübbe, Sabrina
- Environmental Microbiology, Vol. 11, Issue 5
Frequent Mutations within the Genomic Magnetosome Island of Magnetospirillum gryphiswaldense Are Mediated by RecA
journal, October 2011
- Kolinko, Isabel; Jogler, Christian; Katzmann, Emanuel
- Journal of Bacteriology, Vol. 193, Issue 19
Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria
journal, October 1988
- Keen, N. T.; Tamaki, S.; Kobayashi, D.
- Gene, Vol. 70, Issue 1
Genetic plasticity of the Shigella virulence plasmid is mediated by intra- and inter-molecular events between insertion sequences
journal, September 2017
- Pilla, Giulia; McVicker, Gareth; Tang, Christoph M.
- PLOS Genetics, Vol. 13, Issue 9
Genetic changes accompanying increased fitness in evolving populations of Escherichia coli.
journal, February 1992
- Modi, R. I.; Castilla, L. H.; Puskas-Rozsa, S.
- Genetics, Vol. 130, Issue 2
Assembly of G Protein-Coupled Receptors onto Nanosized Bacterial Magnetic Particles Using Mms16 as an Anchor Molecule
journal, May 2004
- Yoshino, Tomoko; Takahashi, Masayoshi; Takeyama, Haruko
- Applied and Environmental Microbiology, Vol. 70, Issue 5
Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle
journal, March 2010
- Murat, D.; Quinlan, A.; Vali, H.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 12
Origin of magnetosome membrane: Proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane
journal, October 2006
- Tanaka, Masayoshi; Okamura, Yoshiko; Arakaki, Atsushi
- PROTEOMICS, Vol. 6, Issue 19
Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals
journal, August 2016
- Arakaki, Atsushi; Kikuchi, Daiki; Tanaka, Masayoshi
- Journal of Bacteriology, Vol. 198, Issue 20
Survival and Evolution of a Large Multidrug Resistance Plasmid in New Clinical Bacterial Hosts
journal, August 2016
- Porse, Andreas; Schønning, Kristian; Munck, Christian
- Molecular Biology and Evolution, Vol. 33, Issue 11
MMS6 Protein Regulates Crystal Morphology during Nano-sized Magnetite Biomineralization in Vivo
journal, December 2010
- Tanaka, Masayoshi; Mazuyama, Eri; Arakaki, Atsushi
- Journal of Biological Chemistry, Vol. 286, Issue 8
Overproduction of Magnetosomes by Genomic Amplification of Biosynthesis-Related Gene Clusters in a Magnetotactic Bacterium
journal, March 2016
- Lohße, Anna; Kolinko, Isabel; Raschdorf, Oliver
- Applied and Environmental Microbiology, Vol. 82, Issue 10
Characterization of the bacterial magnetosome membrane.
journal, January 1988
- Gorby, Y. A.; Beveridge, T. J.; Blakemore, R. P.
- Journal of Bacteriology, Vol. 170, Issue 2
Magnetosome biogenesis in magnetotactic bacteria
journal, September 2016
- Uebe, René; Schüler, Dirk
- Nature Reviews Microbiology, Vol. 14, Issue 10
Immunoassay method for the determination of immunoglobulin G using bacterial magnetic particles
journal, February 1991
- Nakamura, Noriyuki.; Hashimoto, Kohji.; Matsunaga, Tadashi.
- Analytical Chemistry, Vol. 63, Issue 3
Heteromeric transposase elements: generators of genomic islands across diverse bacteria: Heteromeric transposase elements
journal, August 2014
- Peters, Joseph E.; Fricker, Ashwana D.; Kapili, Bennett J.
- Molecular Microbiology
Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK
journal, January 2006
- Komeili, A.
- Science, Vol. 311, Issue 5758
Comparative genomic analysis provides insights into the evolution and niche adaptation of marine Magnetospira sp. QH-2 strain: Comparative genomics of magnetotactic spirilla
journal, July 2013
- Ji, Boyang; Zhang, Sheng-Da; Arnoux, Pascal
- Environmental Microbiology, Vol. 16, Issue 2
Complete Genome Sequence of the Facultative Anaerobic Magnetotactic Bacterium Magnetospirillum sp. strain AMB-1
journal, January 2005
- Matsunaga, T.; Okamura, Y.; Fukuda, Y.
- DNA Research, Vol. 12, Issue 3
The Major Magnetosome Proteins MamGFDC Are Not Essential for Magnetite Biomineralization in Magnetospirillum gryphiswaldense but Regulate the Size of Magnetosome Crystals
journal, October 2007
- Scheffel, André; Gärdes, Astrid; Grünberg, Karen
- Journal of Bacteriology, Vol. 190, Issue 1
Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of Magnetospirillum magneticum AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
journal, September 2017
- Taoka, Azuma; Kiyokawa, Ayako; Uesugi, Chika
- mBio, Vol. 8, Issue 4
Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters
journal, February 2014
- Kolinko, Isabel; Lohße, Anna; Borg, Sarah
- Nature Nanotechnology, Vol. 9, Issue 3
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
Dynamic analysis of a genomic island in Magnetospirillum sp. strain AMB-1 reveals how magnetosome synthesis developed
journal, January 2006
- Fukuda, Yorikane; Okamura, Yoshiko; Takeyama, Haruko
- FEBS Letters, Vol. 580, Issue 3