Biogeochemical Niche of Magnetotactic Cocci Capable of Sequestering Large Polyphosphate Inclusions in the Anoxic Layer of the Lake Pavin Water Column

Abstract

Magnetotactic bacteria (MTB) are microorganisms thriving mostly at oxic–anoxic boundaries of aquatic habitats. MTB are efficient in biomineralising or sequestering diverse elements intracellularly, which makes them potentially important actors in biogeochemical cycles. Lake Pavin is a unique aqueous system populated by a wide diversity of MTB with two communities harbouring the capability to sequester not only iron under the form of magnetosomes but also phosphorus and magnesium under the form of polyphosphates, or calcium carbonates, respectively. MTB thrive in the water column of Lake Pavin over a few metres along strong redox and chemical gradients representing a series of different microenvironments. In this study, we investigate the relative abundance and the vertical stratification of the diverse populations of MTB in relation to environmental parameters, by using a new method coupling a precise sampling for geochemical analyses, MTB morphotype description, and in situ measurement of the physicochemical parameters. We assess the ultrastructure of MTB as a function of depth using light and electron microscopy. We evidence the biogeochemical niche of magnetotactic cocci, capable of sequestering large PolyP inclusions below the oxic–anoxic transition zone. Our results suggest a tight link between the S and P metabolisms of these bacteria and pave the way to better understand the implication of MTB for the P cycle in stratified environmental conditions.

Identification of sulfate‐reducing magnetotactic bacteria via a group‐specific 16S rDNA primer and correlative fluorescence and electron microscopy: Strategy for culture‐independent study

“…A more recent online pumping method (Moskowitz et al, 2008) has been modified for mass MTB cell collection at a defined depth from the permanently stratified ferruginous Lake Pavin, France (Busigny et al, 2022). By using such a system, Bidaud et al (2022) investigated the relative abundance and vertical stratification of diverse MTB populations in relation to environmental parameters and found the biogeochemical niche of magnetotactic cocci, which can sequester large polyphosphate inclusions below the OATZ. These studies provide a new approach for directly concentrating MTB cells and linking their distribution to environmental physicochemical parameters.…”

“…With the assistance of magneto‐aerotaxis/chemotaxis, MTB can efficiently shuttle up toward oxic/microaerobic regions and down toward anaerobic regions in the water column or within sediments (Bazylinski & Trubitsyn, 2019; Li et al, 2020a; Lower & Bazylinski, 2013). Overall, they are an important microbial group that drives biogeochemical cycling of C, N, P, S, Si and Fe within the oxic–anoxic transition zone (OATZ) in aquatic environments (Bidaud et al, 2022; Li et al, 2021; Li et al, 2022b; Monteil et al, 2021; Schulz‐Vogt et al, 2019). For geologists, the fossil remains of MTB (called magnetofossils) preserved in ancient sediments or rocks (i) record ideal magnetic signals for reconstructing paleomagnetic and paleoenvironmental information and (ii) provide reliable biomarkers for indicating the presence of ancient MTB and their related paleoecology (Amor et al, 2020; Chang et al, 2018; Kopp & Kirschvink, 2008; Larrasoaña et al, 2014; Li et al, 2020b; Li et al, 2020c; Yamazaki & Kawahata, 1998).…”

Lake Pavin is a microbial mineralization oasis

“…Here, we propose to review these recent discoveries including the development of a specific sampling strategy of the water column combined with in situ geochemical measurements and microbiology (2). Several models will be introduced, including polyphosphate hyperaccumulating bacteria (3,4) and the broad diversity of MTB ( 5) and non-MTB (6) forming intracellular amorphous carbonates. These results will be discussed as well as the contribution of these microbial mineralization to geochemical cycles of the lake.…”