Cite this paper:
Igor TAVEIRA, Dennis A. BAZYLINSKI, Fernanda ABREU. Release the iron: does the infection of magnetotactic bacteria by phages play a role in making iron available in aquatic environments?[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2063-2069

Release the iron: does the infection of magnetotactic bacteria by phages play a role in making iron available in aquatic environments?

Igor TAVEIRA1, Dennis A. BAZYLINSKI2, Fernanda ABREU1
1 Instituto de Microbiologia Paulo de Góes, Departamento de Microbiologia Geral, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-902, Brazil;
2 School of Life Sciences, University of Nevada at Las Vegas, Las Vegas 94720, USA
Magnetotactic bacteria (MTB) are ubiquitous prokaryotes that orient along magnetic field lines due to magnetosomes’ biomineralization within the cell. These structures are ferrimagnetic organelles that impart a magnetic moment to the cell. To succeed in producing magnetosomes, MTB accumulate iron in (i) cytoplasm; (ⅱ) magnetosomes; and (ⅲ) nearby the organelle. It has already been estimated that a single MTB has an iron content of 10 to 100-fold higher than Escherichia coli. Phages are the most abundant entity in oceans and are known for controlling nutrient flow such as carbon and nitrogen by viral shunt and pump. The current work addresses the putative role of phages that infect MTB on the iron biogeochemical cycle. Can phage infection in MTB hosts cause a biogenic iron fertilization-like event in localized microenvironments? Are phages critical players in driving magnetosome biomineralization genes (BGs) horizontal transfer? Further investigation of those events, including frequency of occurrence, is necessary to fully comprehend MTB’s effect on iron cycling in aqueous environments.
Key words:    horizontal gene transfer|iron biogeochemical cycle|magnetotactic bacteria|magnetosome biomineralization genes|phages   
Received: 2021-03-03   Revised: 2021-04-07
PDF (543 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Igor TAVEIRA
Articles by Dennis A. BAZYLINSKI
Articles by Fernanda ABREU
Akai J, Iida A, Akai K, Chiba A. 1997. Mn and Fe minerals of possible biogenic origin from two Precambrian stromatolites in Western Australia. The Journal of the Geological Society of Japan, 103(5):484-488,
Amor M, Tharaud M, Gélabert A, Komeili A. 2020a. Singlecell determination of iron content in magnetotactic bacteria:implications for the iron biogeochemical cycle. Environmental Microbiology, 22(3):823-831,
Amor M, Mathon F P, Monteil C L, Busigny V, Lefevre C T. 2020b. Iron-biomineralizing organelle in magnetotactic bacteria:function, synthesis and preservation in ancient rock samples. Environmental Microbiology, 22(9):3611-3632,
Bartual S G, Otero J M, Garcia-Doval C, Llamas-Saiz A L, Kahn R, Fox G C, van Raaij M J. 2010. Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proceedings of the National Academy of Sciences of the United States of America, 107(47):20287-20292,
Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nature Reviews Microbiology, 2(3):217-230,
Bonnain C, Breitbart M, Buck K N. 2016. The ferrojan horse hypothesis:iron-virus interactions in the ocean. Frontiers in Marine Science, 3:82, 2016.00082.
Braun V. 2009. FhuA (TonA), the career of a protein. Journal of Bacteriology, 191(11):3431-3436,
Breitbart M, Bonnain C, Malki K, Sawaya N A. 2018. Phage puppet masters of the marine microbial realm. Nature Microbiology, 3(7):754-766,
Browning C, Shneider M M, Bowman V D, Schwarzer D, Leiman P G. 2012. Phage pierces the host cell membrane with the iron-loaded spike. Structure, 20(2):326-339,
Brüssow H, Hendrix R W. 2002. Phage genomics:small is beautiful. Cell, 108(1):13-16,
Butler A. 2005. Marine siderophores and microbial iron mobilization. Biometals, 18(4):369-374,
Chang S B R, Stolz J F, Kirschvink J L, Awramik S M. 1989. Biogenic magnetite in stromatolites. Ⅱ. Occurrence in ancient sedimentary environments. Precambrian Research, 43(4):305-315,
Chen A P, Berounsky V M, Chan M K, Blackford M G, Cady C, Moskowitz B M, Kraal P, Lima E A, Kopp R E, Lumpkin G R, Weiss B P, Hesse P, Vella N G F. 2014. Magnetic properties of uncultivated magnetotactic bacteria and their contribution to a stratified estuary iron cycle. Nature Communications, 5(1):4979,
Clasen J L, Brigden S M, Payet J P, Suttle C A. 2008. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshwater Biology, 53(6):1090-1100,
Clokie M R J, Millard A D, Letarov A V, Heaphy S. 2011. Phages in nature. Bacteriophage, 1(1):31-45,
Cochlan W P, Wikner J, Steward G F, Smith D C, Azam F. 1993. Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments. Marine Ecology Progress Series, 92(1-2):77-87,
Cypriano J, Bahri M, Dembelé K, Baaziz W, Leão P, Bazylinski D A, Abreu F, Ersen O, Farina M, Werckmann J. 2020. Insight on thermal stability of magnetite magnetosomes:implications for the fossil record and biotechnology. Scientific Reports, 10(1):6706,
Danovaro R, Dell'Anno A, Trucco A, Serresi M, Vanucci S. 2001. Determination of virus abundance in marine sediments. Applied and Environmental Microbiology, 67(3):1384-1387,
Dion M B, Oechslin F, Moineau S. 2020. Phage diversity, genomics and phylogeny. Nature Reviews Microbiology, 18(3):125-138,
Erez Z, Steinberger-Levy I, Shamir M, Doron S, StokarAvihail A, Peleg Y, Melamed S, Leavitt A, Savidor A, Albeck S, Amitai G, Sorek R. 2017. Communication between viruses guides lysis-lysogeny decisions. Nature, 541(7638):488-493,
Fantle M S, DePaolo D J. 2004. Iron isotopic fractionation during continental weathering. Earth and Planetary Science Letters, 228(3-4):547-562,
Frankel R B. 1984. Magnetic guidance of organisms. Annual Review of Biophysics and Bioengineering, 13:85-103,
Frankel R B, Blakemore R P. 1980. Navigational compass in magnetic bacteria. Journal of Magnetism and Magnetic Materials, 15-18:1562-1564,
Grant C R, Komeili A. 2020. Ferrosomes are iron storage organelles formed by broadly conserved gene clusters in bacteria and archaea. BioRxiv,
Gregory A C, Zayed A A, Conceição-Neto N, Temperton B, Bolduc B, Alberti A, Ardyna M, Arkhipova K, Carmichael M, Cruaud C, Dimier C, Domínguez-Huerta G, Ferland J, Kandels S, Liu Y X, Marec C, Pesant S, Picheral M, Sunagawa S, Wincker P, Sullivan M B. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell, 177(5):1109-1123, 2019.03.040.
Kavagutti V S, Andrei A Ş, Mehrshad M, Salcher M M, Ghai R. 2019. Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics. Microbiome, 7(1):135,
Kuma K, Nishioka J, Matsunaga K. 1996. Controls on iron(Ⅲ) hydroxide solubility in seawater:the influence of pH and natural organic chelators. Limnology and Oceanography, 41(3):396-407,
Lin W, Bazylinski D A, Xiao T, Wu L F, Pan Y X. 2014. Life with compass:diversity and biogeography of magnetotactic bacteria. Environmental Microbiology, 16(9):2646-2658,
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,
Liu P Y, Liu Y, Zhao X, Roberts A P, Zhang H, Zheng Y, Wang F X, Wang L S, Menguy N, Pan Y X, Li J H. 2021. Diverse phylogeny and morphology of magnetite biomineralized by magnetotactic cocci. Environmental Microbiology, 23(2):1115-1129,
Martin J H, Coale K H, Johnson K S, Fitzwater S E, Gordon R M, Tanner S J, Hunter C N, Elrod V A, Nowicki J L, Coley T L, Barber R T, Lindley S, Watson A J, van Scoy K, Law C S, Liddicoat M I, Ling R, Stanton T, Stockel J, Collins C, Anderson A, Bidigare R, Ondrusek M, Latasa M, Millero F J, Lee K, Yao W, Zhang J Z, Friederich G, Sakamoto C, Chavez F, Buck K, Kolber Z, Greene R, Falkowski P, Chisholm S W, Hoge F, Swift R, Yungel J, Turner S, Nightingale P, Hatton A, Liss P, Tindale N W. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature, 371(6493):123-129,
Martin P, Rosenberg N J, McKenney M S. 1989. Sensitivity of evapotranspiration in a wheat field, a forest, and a grassland to changes in climate and direct effects of carbon dioxide. Climatic Change, 14(2):117-151,
Matzanke B F, Böhnke R, Möllmann U, Reissbrodt R, Schünemann V, Trautwein A X. 1997. Iron uptake and intracellular metal transfer in mycobacteria mediated by xenosiderophores. Biometals, 10(3):193-203,
Parada V, Sintes E, van Aken H M, Weinbauer M G, Herndl G J. 2007. Viral abundance, decay, and diversity in the meso-and bathypelagic waters of the North Atlantic. Applied and Environmental Microbiology, 73(14):4429-4438,
Suttle C A. 2005. Viruses in the sea. Nature, 437(7057):356-361,
Suttle C A. 2007. Marine viruses-major players in the global ecosystem. Nature Reviews Microbiology, 5(10):801-812,
Suttle C A, Chan A M. 1994. Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Applied and Environmental Microbiology, 60(9):3167-3174,
Thiele S, Fuchs B M, Ramaiah N, Amann R. 2012. Microbial community response during the iron fertilization experiment LOHAFEX. Applied and Environmental Microbiology, 78(24):8803-8812,
Werckmann J, Cypriano J, Lefèvre C T, Dembelé K, Ersen O, Bazylinski D A, Lins U, Farina M. 2017. Localized iron accumulation precedes nucleation and growth of magnetite crystals in magnetotactic bacteria. Scientific Reports, 7(1):8291,
Wetzel R G. 2001. Freshwater Ecosystems. 2nd edn. Elsevier, Amsterdam. p.560-569,
Wolfe R S, Thauer R K, Pfennig N. 1987. A ‘capillary racetrack’ method for isolation of magnetotactic bacteria. FEMS Microbiology Ecology, 3(1):31-35,
Yuan W, Zhou H Y, Yang Z Y, Hein J R, Yang Q H. 2020. Magnetite magnetofossils record biogeochemical remanent magnetization in hydrogenetic ferromanganese crusts. Geology, 48(3):298-302,
Copyright © Haiyang Xuebao