Biogeochemical niche of phosphorus sequestrating magnetotactic bacteria in Lake Pavin, a freshwater feruginous environment.

Phosphorus (P) is essential to life but a limiting nutrient in many ecosystems. Understanding the role of microorganisms in P cycling, especially the processes of P uptake and storage, is a major environmental issue.  Only few models are known to highly sequestrate phosphorus and mostly in marine environments. We thus need to improve our knowledge about other model of sequestration and especially in freshwater environments.

Freshwater magnetotactic bacteria (MTB) affiliated to the Magnetococcaceae family have been identified within the water column of Lake Pavin in France [3]. Similarly, to the marine Thiomarguarita and Beggiatoa [1, 2], they accumulate intracellular polyphosphates (PolyP) to a uniquely high extent, up to 90% of their cell volume. In contradiction with the marine Thiomarguarita and Beggiatoa, the Magnetococcaceae accumulate PolyP in anoxic conditions. They represent the major population of MTB and are located right under the oxic-anoxic interface in a zone of strong chemical and redox gradients. These gradients allow the study of the impact of varying chemical conditions on microbial physiology.

We aim at characterizing Magnetococcaceae distribution as a function of depth and therefore of different chemical parameters, but also at determining the drivers of PolyP accumulation. 

Here, we combine a variety of methods to analyse these MTB and their potential appartenance to a specific ecological niche in the water column. We measured the physico-chemical parameters of the water column (O₂, pH, redox, conductivity, FDOM, turbidity, etc.). We used a new sampling system that allowed us to reach a better spatial resolution [4], from 1 m to 20 cm. We were therefore able to better estimate the impact of the chemical parameters on the MTB. We then sampled the water to measure the geochemical parameters using ICP-OES and to characterize MTB via optical and electronic microscopy. Optical microscopy helped identify the main populations of MTB and their concentrations, while electronic microscopy permitted the characterization of the different magnetosome organisation and PolyP accumulation capacities. Multivariate statistics were finally performed on all data.

Multivariate statistics identified several parameters positively and significantly correlated to the Magnetococcaceae. These parameters are different from the ones correlated to other MTB of the water column. We therefore show that the Magnetococcaceae live into a specific niche with specific biogeochemical parameters. These correlated parameters include dissolved lithium concentration, mass percentage of nitrogen, magnesium and particulate P. Phosporus  and magnesium are linked to the formation of PolyP, lithium represent a cofactor for phosphate transport [5] and nitrogen might be linked to nitrate transportation by the MTB [6].

Genomic analyses will be done in the future to allow further comprehension on molecular mecanisms and PolyP formation.

[1] Brock J, Schulz-Vogt HN. (2011) ISME Journal 5, 497-506. [2] Mubmann M et al. (2007) PLoS Biology 5(9), e230. [3] Rivas-Lamelo S et al. (2017) Geochem. Persp. Let. 5, 35–41. [4] Busigny et al., submitted to Environmental Microbiology. [5] Jakobsson E et al. (2017) J. Membr. Biol. 250,587-604. [6] Li et al. (2020) Geophys. Res. Biogeosciences.