Association of magnetotactic multicellular prokaryotes with Pseudoalteromonas species in a natural lagoon environment

Abstract

Magnetotactic bacteria, for the most part, are free-living, motile, unicellular prokaryotes that inhabit almost all marine and freshwater environments. One notable exception to the unicellular mode, however, are the magnetotactic multicellular prokaryotes. These morphologically unique prokaryotes (e.g., Candidatus Magnetoglobus multicellularis) are motile aggregates of 20–40 genetically identical, Gram-negative cells organised as a sphere (or ovoid in shape) and only motile as a unit. No specific close physical association between magnetotactic bacteria and non-magnetotactic microorganisms has ever been reported. Here, using culture-independent approaches, we show an unusual association between the spherical magnetotactic multicellular prokaryote Ca. Magnetoglobus multicellularis and Pseudoalteromonas species in environmental sediment and water samples collected from the Araruama Lagoon in Brazil. Cells of Pseudoalteromonas species were observed to be physically attached to the surface and, notably, even in the intercellular space of these spherical magnetotactic multicellular prokaryotes. An attempt to correlate the frequency of association between Pseudoalteromonas and magnetotactic multicellular prokaryotes with sediment depth was made but only a slight decrease in the number of Pseudoalteromonas cells per magnetotactic multicellular prokaryote was observed with increasing depth. Similar observations were made with magnetotactic multicellular prokaryotes from another Brazilian Lagoon (Rodrigo de Freitas) and the putative symbiont/parasite was detected. Although our results suggest some sort of specificity in the relationship between these prokaryotes, the precise nature of this association remains unclear.

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Acknowledgements

We acknowledge financial support from the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) agencies. D.A.B. is supported by U.S. National Science Foundation grant EAR-1423939. Microscopy Facilities: Unidade de Microscopia Multiusuário Souto-Padrón & Lins (UniMicro, UFRJ) and Centro Nacional de Biologia Estrutural e Bioimagem (CENABIO, UFRJ).

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Correspondence to Fernanda Abreu.

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Figure S1

Scanning electron microscopy of multicellular magnetotactic prokaryotes from Araruama and Rodrigo de Freitas lagoons, Rio de Janeiro, Brazil

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Leão, P., Gueiros-Filho, F.J., Bazylinski, D.A. et al. Association of magnetotactic multicellular prokaryotes with Pseudoalteromonas species in a natural lagoon environment. Antonie van Leeuwenhoek 111, 2213–2223 (2018). https://doi.org/10.1007/s10482-018-1113-x

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Keywords

  • Microbial association
  • Magnetotactic bacteria
  • Magnetosome
  • Magnetotaxis
  • Magnetotactic multicellular prokaryotes