Award Abstract # 1423939
Collaborative Research; Protein Mediated Magnetite Biomineralization

NSF Org: EAR
Division Of Earth Sciences
Recipient: BOARD OF REGENTS OF NEVADA SYSTEM OF HIGHER EDUCATION
Initial Amendment Date: August 26, 2014
Latest Amendment Date: January 17, 2018
Award Number: 1423939
Award Instrument: Standard Grant
Program Manager: Enriqueta Barrera
EAR
 Division Of Earth Sciences
GEO
 Directorate for Geosciences
Start Date: September 1, 2014
End Date: August 31, 2019 (Estimated)
Total Intended Award Amount: $201,878.00
Total Awarded Amount to Date: $242,243.00
Funds Obligated to Date: FY 2014 = $201,878.00
FY 2018 = $40,365.00
History of Investigator:
  • Dennis Bazylinski (Principal Investigator)
    dennis.bazylinski@unlv.edu
Recipient Sponsored Research Office: University of Nevada Las Vegas
4505 S MARYLAND PKWY
LAS VEGAS
NV  US  89154-9900
(702)895-1357
Sponsor Congressional District: 01
Primary Place of Performance: University of Nevada Las Vegas
4505 Maryland Parkway
Las Vegas
NV  US  89154-4004
Primary Place of Performance
Congressional District:
01
Unique Entity Identifier (UEI): DLUTVJJ15U66
Parent UEI: F995DBS4SRN3
NSF Program(s): Geobiology & Low-Temp Geochem
Primary Program Source: 01001415DB NSF RESEARCH & RELATED ACTIVIT
01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 9150
Program Element Code(s): 729500
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

There is increasing demand for magnetic nanoparticles in emerging areas of technology and medicine (e.g., high-density data storage, targeted drug delivery, scaffolding for tissue regeneration). The "ideal" particle for many of these applications is a nanometer scale magnet that has defined shape and morphology, narrow size distribution, high crystallinity, and controlled magnetic direction. Magnetotactic bacteria (MTB) have the innate capacity to synthesize crystals of the mineral magnetite (Fe3O4) that meet all of these criteria. In this proposal, investigators will study the protein-directed crystallization of magnetite by MTB.

MTB exercise strict genetic control over the size, composition, and morphology of their nanomagnetic crystals. Investigators will examine the so-called Mms proteins (Mms-5, 6, 12, 13; or homologues like MamC) to identify the key catalytic domains that direct nucleation and growth of Fe3O4. In vivo biomineralization experiments will be performed using wild-type strains (e.g., Magnetospirillum magneticum) as well as mutationally altered strains generated during this project. In vitro crystallization experiments will be carried out using recombinant proteins, or peptides that mimic key motifs. Structural and magnetic properties of the in vivo vs. in vitro mineral products will be characterized using electron microscopy, atomic force microscopy, confocal laser scanning microscopy, and magnetometry. Those proteins or peptides that catalyze novel mineral products will be further examined using molecular dynamics simulations in silico. The knowledge to be gained from these studies will allow to fabricate nanometer scale, single domain magnetic crystals that are designed to elicit a particular magnetic response.

This project also includes an educational outreach component for middle- and high-school students and teachers. Teachers will spend 3-4 weeks each year with the PIs learning how to collect and isolate MTB from environmental samples as well as characterize MTB with various forms of optical and electron microscopy. Based on this experience, the teachers will design experiments to use in their own classrooms. Investigators will also direct two field camps: an annual, domestic camp on environmental microbiology and one international field camp on biomineralization. Student participants will learn to design and test scientific hypothesis though field studies, lab experiments, and instrumental analyses (e.g., electron microscopy). The students will present their results at an annual science symposium.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 26)
Araújo, A.C., F. Abreu, K. Silva, D.A. Bazylinski, and U. Lins "Magnetotactic bacteria as potential sources of biomaterials and bioproducts" Marine Drugs , v.13 , 2015 , p.389 10.3390/md13010389
Abreu, F., A.C.V. Araujo, P. Leão, K.T. Silva, F. Marques de Carvalho, O. de Lima Cunha, L.G. Almeida, C. Geurink, M. Farina, D. Rodelli, L. Jovane, V.H. Pellizari, A.T. de Vasconcelos, D.A. Bazylinski, and U. Lins. "Culture-independent characterization of novel psychrophilic magnetotactic cocci from Antarctic marine sediments." Environmental Microbiology , v.18 , 2016 , p.4426
Abreu, F., P. Leão, G. Vargas, J. Cypriano, V. Figueiredo, A. Enrich-Prast, D.A. Bazylinski, and U. Lins "Culture-independent characterization of a novel uncultivated magnetotactic member of the Betaproteobacteria class of the Proteobacteria phylum from an acidic lagoon." Environmental Microbiology , v.20 , 2018 , p.2615 10.1111/1462-2920.14286
Araujo, A.C.V., V. Morillo, J. Cypriano, L.C.R.S. Teixeira, P. Leão, S. Lyra, G. de Almeida, D.A. Bazylinski, A.T.R. de Vasconcelos, F. Abreu, and U. Lins. "Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment." BMC Genomics , v.17 , 2016 , p.726
Bazylinski, D.A., V. Morillo, C.T. Lefèvre, N. Viloria, B.L. Dubbels, and T.J. Williams. "Endothiovibrio diazotrophicus gen. nov., sp. nov., a novel nitrogen-fixing, sulfur-oxidizing gammaproteobacterium isolated from a salt marsh." International Journal of Systematic and Evolutionary Microbiology , v.67 , 2017 , p.1491 10.1099/ijsem.0.001743
Cypriano, J., J. Werckmann, G. Vargas, A. Lopes dos Santos, K.T. Silva, P. Leão, F. Almeida. D.A. Bazylinski, M. Farina, U. Lins, and F. Abreu. "Uptake and persistence of bacterial magnetite magnetosomes in a mammalian cell line: implications for medical and biotechnological applications." PLoS One , v.14 , 2019 , p.e0215657 doi.org/10.1371/journal.pone.0215657
Dahoumane, S.A., M. Mechouet, K. Wijesekera, C.D.M. Filipe, C. Sicard, D.A. Bazylinski, and C. Jeffryes "Algae and nanobiotechnology: biosynthesis of inorganic nanoparticles." Green Chemistry , v.19 , 2017 , p.552
Dahoumane, S.A., M. Mechouet, K. Wijesekera, C.D.M. Filipe, C. Sicard, D.A. Bazylinski, and C. Jeffryes. "Algae and nanobiotechnology: biosynthesis of inorganic nanoparticles" Green Chemistry , v.19 , 2017 , p.552 10.1039/C6GC02346K
Descamps, E.C., C.L Monteil, N. Ginet, D. Pignol, D.A Bazylinski, and C.T Lefèvre. "Desulfamplus magnetomortis gen. nov., sp. nov., a magnetotactic bacterium from a brackish desert spring able to biomineralize greigite and magnetite, that represents a novel lineage in the Desulfobacteraceae" Systematic and Applied Microbiology , v.40 , 2017 , p.280 10.1016/j.syapm.2017.05.001.
Du, H., W. Zhang, W. Zhang, W. Zhang, H. Pan, Y. Pan, D.A. Bazylinski, L.-F. Wu, T. Xiao, and W. Lin. "Magnetosome gene duplication as an important driver in the evolution of magnetotaxis in the Alphaproteobacteria." mSystems , v.4 , 2019 , p.e00315-19 DOI: 10.1128/mSystems.00315-19
Leão, P., F.J. Gueiros-Filho, D.A. Bazylinski, U. Lins, and F. Abreu "Association of magnetotactic multicellular prokaryotes with Pseudoalteromonas species in a natural lagoon environment" Antonie van Leeuwenhoek , v.111 , 2018 , p.2213 10.1007/s10482-018-1113-x
(Showing: 1 - 10 of 26)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Intellectual Merit: Magnetotactic bacteria are a very diverse group of motile (swimming) bacteria that synthesize internal crystals of a magnetic mineral called magnetosomes. These structures cause cells of these organisms to align and swim along the Earth’s geomagnetic field lines like living, miniature, swimming compass needles. Funding from the proposal allowed us to isolate and grow and thus study in detail a number of new magnetotactic bacterial species. Data from these studies resulted in some new and novel findings.

Comparative genomic DNA sequencing studies, in particular, resulted in the following findings: 1) Magnetotactic bacteria appear to represent an ancient group of bacteria and our studies indicate that they existed in the Archean era (4 to 2.5 billion years ago) and were thus likely the first organisms to synthesize minerals for a purpose (i.e., controlled biomineralization) and the first organisms to use the Earth’s magnetic field for navigation (magnetoreception). 2) Magnetotactic bacteria belong to several different evolutionary groups of bacteria. We have now sequenced genomic DNA from magnetotactic bacteria from all these groups. Surprisingly, there were significant differences in the magnetosome genes from bacteria of these different groups. For example, we initially focused our study partially on the mms genes found in some magnetotactic bacteria and their role in biomineralization (see below). We now know that many magnetotactic species from different evolutionary groups do not possess these genes. In addition to this type of difference, we have found some important correlations between the mineral composition and morphology of magnetosome crystals in these different groups that also appears to be linked to the relative “age” of the group. In other words, magnetotactic bacteria from specific group will produce magnetosome crystals of a specific composition and crystal shape. Briefly, it appears that the iron oxide magnetite (Fe3O4) (versus greigite, Fe3S4) was the first mineral to be formed by magnetotactic bacteria and the morphology of the crystals was bullet-shaped. Later evolutionary groups of magnetotactic bacteria also synthesize magnetite but instead of bullet-shaped crystals, these organisms produced rough cuboidal or elongated crystals resembling rectangles. Greigite production, thus far, was only found in one evolutionary group that also process bullet-shaped crystals of magnetite and may be the result of the duplication of certain magnetosome genes that allowed some of the genes to evolve for another process, in this case, greigite formation. This information is important as it helps us to understand how we may be able to determine whether certain types of magnetite and/or greigite crystals found in ancient sediments and extraterrestrial materials such as meteorites are biogenic in origin. That is, can these latter crystals be used as “magnetofossils”, the remnants of dead magnetotactic bacteria? This has been a very controversial subject in the last few decades and research is sorely needed on this topic. 3) In conjunction with 2, we also examined magnetosome magnetite crystals from a magnetotactic bacterium at the molecular level using a new very sensitive technique known as atomic probe tomography. We found trace levels of carbon within the actual structure of the magnetite crystal. Carbon was not present in magnetites produced inorganically (chemically). These results suggest that maybe this carbon signature can be used as biomarker for biologically-produced magnetites thereby confirming whether a magnetite crystal is biogenic and a true magnetofossil from magnetotactic bacteria. 4) As stated above, we initially proposed to study the functions of a group of magnetosome genes called the mms genes. Our results suggest that at least some of these genes are involved in controlling the size and shape of magnetosome magnetite crystals in some magnetotactic bacteria. 4)

Broader impacts: Funding from this grant provided opportunities, training and professional development for three international postdoctoral scholars, one doctoral graduate student and numerous undergraduates who worked on parts of this project.

Data from this work (e.g., genomic DNA sequences) have been deposited into databases for access to all who are interested and thus the data has been disseminated widely.

The impact of our results range broadly. Findings/results from this study made a significant impact on not only in microbiology but also in biomineralization, chemistry, geochemistry, geology, paleomagnetism and magnetoreception in biological organisms. In addition, understanding the biomineralization processes and mechanisms involved in magnetosome formation and how magnetotaxis originated might have a profound effect on the understanding of the evolution of bacteria on Earth in general.


Last Modified: 12/19/2019
Modified by: Dennis A Bazylinski

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