Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain

Rozalyn A. SIMON; Purnika Damindi RANASINGHE; Nawroz BARAZANJI; Malin Bergman JUNGESTRÖM; Jie XU; Olga BEDNARSKA; Lena SERRANDER; Maria ENGSTRÖM; Dennis A. BAZYLINSKI; Åsa V. KEITA; Susanna WALTER

doi:10.1007/s00343-021-0495-1

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Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain

Special Section: Magnetotactic Bacteria and Magnetoreception | Updated：2023-05-20

- Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain
- Journal of Oceanology and Limnology Vol. 39, Issue 6, Pages: 2044-2052(2021)
- Affiliations：
  
  1.Center for Medical Image Science and Visualization(CMIV), Linköping University, Linköping 58183, Sweden
  2.Department of Health, Medicine, and Caring Sciences, Linko?ping University, Linko?ping 58183, Sweden
  3.Division of Infection and Inflammation, Department of Biomedical and Clinical Sciences, Linköping University, Linköping 58183, Sweden
  4.Institute of Global Food Security, School of Biological Sciences, Queen's University Belfast, Belfast BT95 DL, United Kingdom
  5.School of Life Sciences, University of Nevada at Las Vegas, Las Vegas, Nevada 89154, USA
  6.Division of Surgery, Orthopedics and Oncology, Department of Clinical and Experimental Medicine, Linköping University, Linköping 58183, Sweden
- Author bio：
  
  Rozalyn A. SIMON, rozalyn.simon@liu.se
- Funds：
- DOI：10.1007/s00343-021-0495-1
  CLC：
- Received：31 December 2020，
  
  Accepted：23 February 2021，
  
  Online First：08 April 2021，
  
  Published：2021-11
- Accepted：
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Rozalyn A. SIMON, Purnika Damindi RANASINGHE, Nawroz BARAZANJI, et al. Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2044-2052.
DOI：

Rozalyn A. SIMON, Purnika Damindi RANASINGHE, Nawroz BARAZANJI, et al. Magnetotactic bacteria from the human gut microbiome associated with orientation and navigation regions of the brain[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2044-2052. DOI： 10.1007/s00343-021-0495-1.

摘要

Abstract

Magnetotactic bacteria (MTB)

ubiquitous in soil and fresh and saltwater sources have been identified in the microbiome of humans and many animals. MTB endogenously produce magnetic nanocrystals enabling them to orient and navigate along geomagnetic fields. Similar magnetite deposits have been found throughout the tissues of the human brain

including brain regions associated with orientation such as the cerebellum and hippocampus

the origins of which remain unknown. Speculation over the role and source of MTB in humans

as well as any association with the brain

remain unanswered. We performed a metagenomic analysis of the gut microbiome of 34 healthy females as well as grey matter volume analysis in magnetite-rich brain regions associated with orientation and navigation with the goal of identifying specific MTB that could be associated with brain structure in orientation and navigation regions. We identified seven MTB in the human gut microbiome:

Magnetococcus marinus

Magnetospira

sp. QH-2

Magnetospirillum

magneticum

Magnetospirillum

sp. ME-1

Magnetospirillum

sp. XM-1

Magnetospirillum gryphiswaldense

and

Desulfovibrio magneticus

. Our preliminary results show significant negative associations between multiple MTB with bilateral flocculonodular lobes of the cerebellum and hippocampus (adjusted for total intracranial volume

uncorrected

0.05). These findings indicate that MTB in the gut are associated with grey matter volume in magnetite-rich brain regions related to orientation and navigation. These preliminary findings support MTB as a potential biogenic source for brain magnetite in humans. Further studies will be necessary to validate and elucidate the relationship between these bacteria

magnetite concentrations

and brain function.

关键词

Keywords

references

Aitchison J. 1982. The statistical analysis of compositional data. Journal of the Royal Statistical Society : Series B ( Methodological ), 44 (2): 139-160, https://doi.org/10.1111/j.2517-6161.1982.tb01195.x..

Al-Obaidi M M J, Desa M N M. 2018. Mechanisms of blood brain barrier disruption by different types of bacteria, and bacterial-host interactions facilitate the bacterial pathogen invading the brain. Cellular and Molecular Neurobiology , 38 (7): 1349-1368, https://doi.org/10.1007/s10571-018-0609-2..

Andrade J C, Almeida D, Domingos M, Seabra C L, Machado D, Freitas A C, Gomes A M. 2020. Commensal obligate anaerobic bacteria and health: production, storage, and delivery strategies. Frontiers in Bioengineering and Biotechnology , 8 : 550, https://doi.org/10.3389/fbioe.2020.00550..

Ashburner J, Friston K J. 2000. Voxel-based morphometry— the methods. NeuroImage , 11 (6): 805-821, https://doi.org/10.1006/nimg.2000.0582..

Ashburner J. 2007. A fast diffeomorphic image registration algorithm. NeuroImage , 38 (1): 95-113, https://doi.org/10.1016/j.neuroimage.2007.07.007..

Bazylinski D A, Frankel R B, Konhauser K O. 2007. Modes of biomineralization of magnetite by microbes. Geomicrobiology Journal , 24 (6): 465-475, https://doi.org/10.1080/01490450701572259..

Bazylinski D A, Williams T J, Lefèvre C T, Berg R J, Zhang C L, Bowser S S, Dean A J, Beveridge T J. 2013. Magnetococcus marinus gen. nov., sp. nov., a marine, magnetotactic bacterium that represents a novel lineage ( Magnetococcaceae fam. nov., Magnetococcales ord. nov. ) at the base of the Alphaproteobacteria. International Journal of Systematic and Evolutionary Microbiology , 63 : 801-808, https://doi.org/10.1099/ijs.0.038927-0..

Bazylinski D, Lefèvre C. 2013. Magnetotactic bacteria from extreme environments. Life , 3 (2): 295-307, https://doi.org/10.3390/life3020295..

Bednarska O, Walter S A, Casado-Bedmar M, Ström M, SalvoRomero E, Vicario M, Mayer E A, Keita Å V. 2017. Vasoactive intestinal polypeptide and mast cells regulate increased passage of colonic bacteria in patients with irritable bowel syndrome. Gastroenterology , 153 (4): 948-960. e3, https://doi.org/10.1053/j.gastro.2017.06.051..

Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics , 30 (15): 2114-2120, https://doi.org/10.1093/bioinformatics/btu170..

Branton W G, Ellestad K K, Maingat F, Wheatley B M, Rud E, Warren R L, Holt R A, Surette M G, Power C. 2013. Brain microbial populations in HIV/AIDS: α-Proteobacteria predominate independent of host immune status. PLoS One , 8 (1): e54673, https://doi.org/10.1371/journal.pone.0054673..

Brem F, Tiefenauer L, Fink A, Dobson J, Hirt A M. 2006. A mixture of ferritin and magnetite nanoparticles mimics the magnetic properties of human brain tissue. Physical Review B , 73 (22): 224427, https://doi.org/10.1103/PhysRevB.73.224427..

Buchfink B, Xie C, Huson D H. 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods , 12 (1): 59-60, https://doi.org/10.1038/nmeth.3176..

Calle M L. 2019. Statistical analysis of metagenomics data. Genomics & Informatics , 17 (1): e6, https://doi.org/10.5808/GI.2019.17.1.e6..

Collingwood J, Dobson J. 2006. Mapping and characterization of iron compounds in Alzheimer's tissue. Journal of Alzheimer ' s Disease , 10 (2-3): 215-222, https://doi.org/10.3233/JAD-2006-102-308..

Daugherty A M, Haacke E M, Raz N. 2015. Striatal iron content predicts its shrinkage and changes in verbal working memory after two years in healthy adults. Journal of Neuroscience , 35 (17): 6731-6743, https://doi.org/10.1523/JNEUROSCI.4717-14.2015..

Daugherty A M, Raz N. 2016. Accumulation of iron in the putamen predicts its shrinkage in healthy older adults: a multi-occasion longitudinal study. NeuroImage , 128 : 11-20, https://doi.org/10.1016/j.neuroimage.2015.12.045..

Dobson J. 2002. Investigation of age-related variations in biogenic magnetite levels in the human hippocampus. Experimental Brain Research , 144 (1): 122-126, https://doi.org/10.1007/s00221-002-1066-0..

Dunn J R, Fuller M, Zoeger J, Dobson J, Heller F, Hammann J, Caine E, Moskowitz B M. 1995. Magnetic material in the human hippocampus. Brain Research Bulletin , 36 (2): 149-153, https://doi.org/10.1016/0361-9230(94)00182-Z..

Gieré R. 2016. Magnetite in the human body: biogenic vs. anthropogenic. Proceedings of the National Academy of Sciences of the United States of America , 113 (43): 11986-11987, https://doi.org/10.1073/pnas.1613349113..

Gilder S A, Wack M, Kaub L, Roud S C, Petersen N, Heinsen H, Hillenbrand P, Milz S, Schmitz C. 2018. Distribution of magnetic remanence carriers in the human brain. Scientific Reports , 8 (1): 11363, https://doi.org/10.1038/s41598-018-29766-z..

Gloor G B, Wu J R, Pawlowsky-Glahn V, Egozcue J J. 2016. It's all relative: analyzing microbiome data as compositions. Annals of Epidemiology , 26 (5): 322-329, https://doi.org/10.1016/j.annepidem.2016.03.003..

Gorobets O, Gorobets S, Koralewski M. 2017a. Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans. International Journal of Nanomedicine , 12 : 4371-4395, https://doi.org/10.2147/IJN.S130565..

Gorobets S V, Gorobets O Y, Medviediev O V, Golub V O, Kuzminykh L V. 2017b. Biogenic magnetic nanoparticles in lung, heart and liver. Functional Materials , 24 (3): 405-408, https://doi.org/10.15407/fm24.03.405..

Gorobets S V, Gorobets O Y. 2012. Functions of biogenic magnetic nanoparticles in organisms. Functional Materials , 19 (1): 18-26..

Gorobets S V, Medviediev O, Gorobets O Y, Ivanchenko A. 2018. Biogenic magnetic nanoparticles in human organs and tissues. Progress in Biophysics and Molecular Biology , 135 : 49-57..

Gupta A, Kilpatrick L, Labus J, Tillisch K, Braun A, Hong J Y, Ashe-McNalley C, Naliboff B, Mayer E A. 2014. Early adverse life events and resting state neural networks in patients with chronic abdominal pain: evidence for sex differences. Psychosomatic Medicine , 76 (6): 404-412, https://doi.org/10.1097/PSY.0000000000000089..

Gupta A, Mayer E A, Fling C, Labus J S, Naliboff B D, Hong J Y, Kilpatrick L A. 2017. Sex-based differences in brain alterations across chronic pain conditions. Journal of Neuroscience Research , 95 (1-2): 604-616, https://doi.org/10.1002/jnr.23856..

Haines D E, Mihailoff G A. 2018. The cerebellum. In : Fundamental Neuroscience for Basic and Clinical Applications. 5th edn. Elsevier, Philadelphia, PA. p. 394-412. e1.

Hautot D, Pankhurst Q A, Khan N, Dobson J. 2003. Preliminary evaluation of nanoscale biogenic magnetite in Alzheimer's disease brain tissue. Proceedings of the Royal Society of London . Series B : Biological Sciences , 270 (Suppl. 1): S62-S64, https://doi.org/10.1098/rsbl.2003.0012..

Huerta-Cepas J, Forslund K, Coelho L P, Szklarczyk D, Jensen L J, von Mering C, Bork P. 2017. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Molecular Biology and Evolution , 34 (8): 2115-2122, https://doi.org/10.1093/molbev/msx148..

Khan S, Chang R. 2013. Anatomy of the vestibular system: a review. NeuroRehabilitation , 32 (3): 437-443, https://doi.org/10.3233/NRE-130866..

Khan S, Cohen D. 2019. Using the magnetoencephalogram to noninvasively measure magnetite in the living human brain. Human Brain Mapping , 40 (5): 1654-1665, https://doi.org/10.1002/hbm.24477..

Kirschvink J L, Kobayashi-Kirschvink A, Woodford B J. 1992. Magnetite biomineralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America , 89 (16): 7683-7687, https://doi.org/10.1073/pnas.89.16.7683..

Laurens J, Angelaki D E. 2016. How the vestibulocerebellum builds an internal model of self-motion. In : The Neuronal Codes of the Cerebellum. Elsevier, London. p. 97-115.

Lê Cao K A, Costello M E, Lakis V A, Bartolo F, Chua X Y, Brazeilles R, Rondeau P. 2016. MixMC: a multivariate statistical framework to gain insight into microbial communities. PLoS One , 11 (8): e0160169, https://doi.org/10.1371/journal.pone.0160169..

Li D H, Liu C M, Luo R B, Sadakane K, Lam T W. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics , 31 (10): 1674-1676, https://doi.org/10.1093/bioinformatics/btv033..

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics , 25 (14): 1754-1760, https://doi.org/10.1093/bioinformatics/btp324..

Lin W, Pan Y X, Bazylinski D A. 2017. Diversity and ecology of and biomineralization by magnetotactic bacteria. Environmental Microbiology Reports , 9 (4): 345-356, https://doi.org/10.1111/1758-2229.12550..

Maher B A, Ahmed I A M, Karloukovski V, MacLaren D A, Foulds P G, Allsop D, Mann D M A, Torres-Jardón R, Calderon-Garciduenas L. 2016. Magnetite pollution nanoparticles in the human brain. Proceedings of the National Academy of Sciences of the United States of America , 113 (39): 10797-10801, https://doi.org/10.1073/pnas.1605941113..

Maher B A. 2019. Airborne magnetite- and iron-rich pollution nanoparticles: potential neurotoxicants and environmental risk factors for neurodegenerative disease, including Alzheimer's disease. Journal of Alzheimer ' s Disease , 71 (2): 361-375, https://doi.org/10.3233/JAD-190204..

Medviediev O, Gorobets O Y, Gorobets S V, Yadrykhins'ky V S. 2017. The prediction of biogenic magnetic nanoparticles biomineralization in human tissues and organs. Journal of Physics : Conference Series , 903 : 012002, https://doi.org/10.1088/1742-6596/903/1/012002..

Modica C M, Zivadinov R, Dwyer M G, Bergsland N, Weeks A R, Benedict R H B. 2015. Iron and volume in the deep gray matter: association with cognitive impairment in multiple sclerosis. American Journal of Neuroradiology , 36 (1): 57-62, https://doi.org/10.3174/ajnr.A3998..

Natan E, Fitak R R, Werber Y, Vortman Y. 2020. Symbiotic magnetic sensing: raising evidence and beyond: symbiotic magnetic sensing. Philosophical Transactions of the Royal Society B : Biological Sciences , 375 (1808): 20190595, https://doi.org/10.1098/rstb.2019.0595rstb20190595..

Natan E, Vortman Y. 2017. The symbiotic magnetic-sensing hypothesis: do Magnetotactic bacteria underlie the magnetic sensing capability of animals? Movement Ecology , 5 (1): 22, https://doi.org/10.1186/s40462-017-0113-1..

Pankhurst Q, Hautot D, Khan N, Dobson J. 2008. Increased levels of magnetic iron compounds in Alzheimer's disease. Journal of Alzheimer ' s Disease , 13 (1): 49-52, https://doi.org/10.3233/JAD-2008-13105..

Plascencia-Villa G, Ponce A, Collingwood J F, ArellanoJiménez M J, Zhu X W, Rogers J T, Betancourt I, José-Yacamán M, Perry G. 2016. High-resolution analytical imaging and electron holography of magnetite particles in amyloid cores of Alzheimer's disease. Scientific Reports , 6 (1): 24873, https://doi.org/10.1038/srep24873..

Roberts R C, Farmer C B, Walker C K. 2018. The human brain microbiome; there are bacteria in our brains! In : Society for Neuroscience Meeting. San Diego.

Rochefort C, Lefort J M, Rondi-Reig L. 2013. The cerebellum: a new key structure in the navigation system. Frontiers in Neural Circuits , 7 : 35, https://doi.org/10.3389/fncir.2013.00035..

Rodrigue K M, Daugherty A M, Haacke E M, Raz N. 2013. The role of hippocampal iron concentration and hippocampal volume in age-related differences in memory. Cerebral Cortex , 23 (7): 1533-1541, https://doi.org/10.1093/cercor/bhs139..

Salami A, Papenberg G, Sitnikov R, Laukka E J, Persson J, Kalpouzos G. 2021. Elevated neuroinflammation contributes to the deleterious impact of iron overload on brain function in aging. NeuroImage , 230 : 117792, https://doi.org/10.1016/j.neuroimage.2021.117792..

Santos-Marcos J A, Rangel-Zuñiga O A, Jimenez-Lucena R, Quintana-Navarro G M, Garcia-Carpintero S, Malagon M M, Landa B B, Tena-Sempere M, Perez-Martinez P, Lopez-Miranda J, Perez-Jimenez F, Camargo A. 2018. Influence of gender and menopausal status on gut microbiota. Maturitas , 116 (8): 43-53, https://doi.org/10.1016/j.maturitas.2018.07.008..

Schultheiss-Grassi P P, Wessiken R, Dobson J. 1999. TEM investigations of biogenic magnetite extracted from the human hippocampus. Biochimica et Biophysica Acta ( BBA ): General Subjects , 1426 (1): 212-216, https://doi.org/10.1016/S0304-4165(98)00160-3..

Shin J H, Park Y H, Sim M, Kim S A, Joung H, Shin D M. 2019. Serum level of sex steroid hormone is associated with diversity and profiles of human gut microbiome. Research in Microbiology , 170 (4-5): 192-201, https://doi.org/10.1016/j.resmic.2019.03.003..

Wang C X, Hilburn I A, Wu D A, Mizuhara Y, Cousté C P, Abrahams J N H, Bernstein S E, Matani A, Shimojo S, Kirschvink J L. 2019. Transduction of the geomagnetic field as evidenced from alpha-band activity in the human brain. eNeuro , 6 (2): ENEURO.0483-18.2019, https://doi.org/10.1523/ENEURO.0483-18.2019..

Wood D E, Salzberg S L. 2014. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biology , 15 (3): R46, https://doi.org/10.1186/gb-2014-15-3-r46..

Yakusheva T A, Blazquez P M, Chen A, Angelaki D E. 2013. Spatiotemporal properties of optic flow and vestibular tuning in the cerebellar nodulus and uvula. The Journal of Neuroscience , 33 (38): 15145-15160, https://doi.org/10.1523/JNEUROSCI.2118-13.2013..

Zhao H, Chen J J, Li X P, Sun Q, Qin P P, Wang Q. 2019. Compositional and functional features of the female premenopausal and postmenopausal gut microbiota. FEBS Letters , 593 (18): 2655-2664, https://doi.org/10.1002/1873-3468.13527..

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