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

Nicolas Menguy,Fériel Skouri-Panet,Élodie Duprat,Cécile C Bidaud,Christopher T Lefevre,Vincent Busigny,Didier Jézéquel,Cynthia Travert,Éric Viollier,Karim Benzerara,Caroline L Monteil

doi:10.3389/fmicb.2021.789134

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.

Highlights

Magnetotactic bacteria (MTB) refer to a unique group of morphologically, phylogenetically, and physiologically diverse microorganisms thriving mostly at oxic–anoxic boundaries of aquatic habitats
MTB observed at the oxic–anoxic transition zone (OATZ) in the stratified water column and in sediments of the ferruginous Lake Pavin (Massif Central, France) harbour the capability to sequester phosphorus and cations (Ca2+, Mg2+, or K+) in the form of very large inclusions of polyphosphates (PolyP), or carbon and calcium in the form of amorphous calcium carbonates (RivasLamelo et al, 2017; Monteil et al, 2021)
The physicochemical profile acquired on the first day in Lake Pavin allowed us to localise the OATZ and MTB communities in the water column (Figure 1)

Summary

Introduction

Magnetotactic bacteria (MTB) refer to a unique group of morphologically, phylogenetically, and physiologically diverse microorganisms thriving mostly at oxic–anoxic boundaries of aquatic habitats. Previous studies showed that phosphogenesis in this lake occurs just beneath the OATZ (Busigny et al, 2016) and suggested the involvement of cells in mineral precipitations (Cosmidis et al, 2014; Miot et al, 2016) In this freshwater environment, magnetotactic cocci (MTBc) hyperaccumulating P (up to 90% of their cell volume) as intracellular PolyP were affiliated to the Magnetococcaceae family of the Candidatus Betaproteobacteria class— proposed as the class Magnetococcia in the GTDB taxonomy (Ji et al, 2017; Parks et al, 2018). Only Cyanobacteria and the non-magnetotactic Gammaproteobacterium Achromatium were known to form carbonate phases in undersaturated solutions (Head et al, 1996; Couradeau et al, 2012; Salman et al, 2015; Cam et al, 2016; Benzerara et al, 2020)

Methods

Results

Conclusion