Magnetotactic bacteria and magnetofossils: ecology, evolution and environmental implications

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Evolution has bestowed life on Earth with some amazing senses, but one of the least understood among them is magnetoreception. Despite convincing behavioural evidence in support of magnetoreception, it has been difficult, so far, to pinpoint a particular set of genes solely responsible for this sensory transduction. So how do life detect Earth’s magnetic field still remains a topic of particular interest. Magnetoreception has been a case of fascination among biologists, physicists and geologists alike, for more than half a century.

Magnetoreception and magnetotactic bacteria

Magnetotactic bacteria (MTB) are a group of phylogenetically diverse and morphologically varied microorganisms with a magnetoresponsive capability called magnetotaxis or microbial magnetoreception. MTB are a distinctive constituent of the microbiome of aquatic ecosystems because they use Earth’s magnetic field to align themselves in a north or south facing direction and efficiently navigate to their favoured microenvironments. Magnetoreception represents a spectrum of capabilities of which magnetotaxis is a subset. While magnetoreception is mostly associated with higher organisms that use a magnetic sense for mobility, magnetotaxis is associated with microorganisms. It is related to previously discovered methods of taxis such as chemotaxis and aerotaxis, which are common modes of transportation and translocation by bacteria and archaea [1,2]. However, unlike chemotaxis or aerotaxis, which are multidirectional, magnetotaxis mostly involves upward/downward movement in search of optimal microenvironments near chemical gradients in water/sediment, aligning passively along Earth’s magnetic field [3]. It is thought that magnetotaxis along with chemotaxis/aerotaxis provides an additional benefit to MTB by permitting an efficient, one-dimensional search along the oxic–anoxic interface (OAI) in aquatic environments to enable MTB to find optimal oxygen concentrations to carry out necessary physiological functions [4].

Transmission electron microscopy images of magnetotactic bacteria with varying morphology. The arrows point at magnetosome chains within the cells.

MTB were first described by Bellini in 1963 [5]. They were collected from various freshwater environments near Pavia, Italy. He observed that a large number of bacteria doggedly swam in a northward direction and this led him to speculate that some sort of “magnetic compass” was behind this kind of movement. In the year 1974, at the Woods Hole Oceanographic Institution in Massachusetts, Blakemore, a pioneer in the field of studying magnetotactic bacteria, suggested that in certain bacteria, magnetite (Fe3O4) which is an ore of iron, acts as a magnetic sensor. On studying these bugs from Cape Cod marsh muds, Blakemore observed that they moved in the direction of magnets when he puts a magnet next to a glass slide containing them [6]. On following up with TEM analysis, he found that these bugs contained chains of magnetite nanoparticles in them which enabled them to align with the Earth’s magnetic field. According to norm, bacteria mostly find the optimal oxygen and nutrients by utilising a “tumble and run” mechanism called chemotaxis. But Blakemore’s magnetotactic bacteria took advantage of the Earth’s magnetic field for motility and it is termed as magnetotaxis. Blakemore independently rediscovered MTB in 1974 and was the first to demonstrate Bellini’s “magnetic compass”- now known as the magnetosomes [7], that are biomineralized within cells of MTB.

Why MTB?

MTB have been identified worldwide from diverse aquatic and waterlogged microbiomes, including freshwater, saline, brackish and marine ecosystems, and some extreme environments. MTB play important roles in the biogeochemical cycling of iron, sulphur, phosphorus, carbon and nitrogen in nature and have been recognized from in vitro cultures to sequester heavy metals like selenium, cadmium and tellurium, which makes them prospective candidate organisms for aquatic pollution bioremediation.

Magnetotaxis, combined with chemotaxis and aerotaxis, allows MTB to efficiently locate and maintain an optimal position for survival and growth in habitats with vertical redox concentration gradients in water columns and sediments.

The role of MTB in environmental systems is not limited to their lifespan; after death, fossil magnetosomal magnetic nanoparticles (known as magnetofossils) are a promising proxy for recording paleoenvironmental change and geomagnetic field history. Recent developments of omics, cultivation and magnetic measurements have expanded our understanding of MTB and magnetofossils. Multiple studies have pointed out that magnetotaxis is monophyletic in origin; that is, it originated from a single common ancestor [8,9,10]. This would make it a primordial physiological phenomenon and (probably) the earliest case of magnetoreception and systematic biomineralization on Earth [11,12]. Following this discovery, diverse multidisciplinary studies have sought to answer several significant questions. Are MTB widespread across the domain Bacteria? How did magnetotaxis originate and evolve? Do MTB have a significant role in biogeochemical element cycling? These questions are of multidisciplinary interest to microbiologists, geologists, physicists, and chemists. In this paper, we summarize the ecology, diversity, evolution, and environmental function of MTB and the paleoenvironmental implications of magnetofossils in light of recent discoveries. Moreover, we discuss expanding oxygen minimum zones (OMZs) in the oceans; diverse MTB likely live in OMZs and their environmental role in such settings has been understudied.

 References:

[1]   Adler, J. Chemotaxis in bacteria. Science 153, 708–716 (1966).  

[2]   Koshland, D. E. A model regulatory system: bacterial chemotaxis. Physiol. Rev. 59, 811–862 (1979).

[3]   Bazylinski, D. A. & Frankel, R. B. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2, 217–230 (2004).

[4]   Mao, X., Egli, R., Petersen, N., Hanzlik, M. & Liu, X. Magneto-chemotaxis in sediment: first insights. PLoS ONE 9, e102810 (2014).

[5]   Bellini, S. On a unique behavior of freshwater bacteria. Chin. J. Oceanol. Limnol. 27, 3–5 (2009).

[6]   Blakemore, R. P. Magnetotactic bacteria. Science 190, 377–379 (1975).

[7]   Balkwill, D. L., Maratea, D. & Blakemore, R. P. Ultrastructure of a magnetic spirillum. J. Bacteriol. 141, 1399–1408 (1980)

[8] Abreu, F. et al. Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria. ISME J. 5, 1634–1640 (2011).

[9] Lefèvre, C. T. et al. Monophyletic origin of magnetotaxis and the first magnetosomes. Environ. Microbiol. 15, 2267–2274 (2013).

[10]   Lin, W. et al. Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. ISME J. 12, 1508–1519 (2018).

[11] Lin, W., Kirschvink, J. L., Paterson, G. A., Bazylinski, D. A. & Pan, Y. On the origin of microbial magnetoreception. Natl Sci. Rev. 7, 472–479 (2020).

[12] Lin, W. et al. Origin of microbial biomineralization and magnetotaxis during the Archean. Proc. Natl Acad. Sci. USA 114, 2171–2176 (2017).

Pranami Goswami

Doctoral candidate, University of Chinese Academy of Sciences/ Australian National University

I am a dual-PhD candidate at the University of Chinese Academy of Sciences and Australian National University. I am studying the phylogenomics of magnetotactic bacteria.