Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin

PLoS One. 2019 Feb 22;14(2):e0212787. doi: 10.1371/journal.pone.0212787. eCollection 2019.

Abstract

Both iron- and sulfur- reducing bacteria strongly impact the mineralogy of iron, but their activity has long been thought to be spatially and temporally segregated based on the higher thermodynamic yields of iron over sulfate reduction. However, recent evidence suggests that sulfur cycling can predominate even under ferruginous conditions. In this study, we investigated the potential for bacterial iron and sulfur metabolisms in the iron-rich (1.2 mM dissolved Fe2+), sulfate-poor (< 20 μM) Lake Pavin which is expected to host large populations of iron-reducing and iron-oxidizing microorganisms influencing the mineralogy of iron precipitates in its permanently anoxic bottom waters and sediments. 16S rRNA gene amplicon libraries from at and below the oxycline revealed that highly diverse populations of sulfur/sulfate-reducing (SRB) and sulfur/sulfide-oxidizing bacteria represented up to 10% and 5% of the total recovered sequences in situ, respectively, which together was roughly equivalent to the fraction of putative iron cycling bacteria. In enrichment cultures amended with key iron phases identified in situ (ferric iron phosphate, ferrihydrite) or with soluble iron (Fe2+), SRB were the most competitive microorganisms, both in the presence and absence of added sulfate. The large fraction of Sulfurospirillum, which are known to reduce thiosulfate and sulfur but not sulfate, present in all cultures was likely supported by Fe(III)-driven sulfide oxidation. These results support the hypothesis that an active cryptic sulfur cycle interacts with iron cycling in the lake. Analyses of mineral phases showed that ferric phosphate in cultures dominated by SRB was transformed to vivianite with concomitant precipitation of iron sulfides. As colloidal FeS and vivianite have been reported in the monimolimnion, we suggest that SRB along with iron-reducing bacteria strongly influence iron mineralogy in the water column and sediments of Lake Pavin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ferrous Compounds / metabolism*
  • Lakes / microbiology*
  • Phosphates / metabolism*
  • Sulfates / metabolism*
  • Sulfides / metabolism*
  • Sulfur-Reducing Bacteria / classification
  • Sulfur-Reducing Bacteria / genetics
  • Sulfur-Reducing Bacteria / metabolism*
  • Water Microbiology*

Substances

  • Ferrous Compounds
  • Phosphates
  • Sulfates
  • Sulfides
  • ferrous phosphate

Grants and funding

JSB was funded by Labex MATISSE, supported by French state funds managed by the Agence Nationale de la Recherche (ANR) within the Investissements d'Avenir programme under reference ANR-11-IDEX-0004-02, and more specifically within the framework of the Cluster of Excellence MATISSE led by Sorbonne Universités. We acknowledge support from the ANR (project SRB – ANR-14-CE33-0003-01, PI: JM). The SEM facility at the IMPMC is funded by Région Ile de France grant SESAME 2006 N°I-07-593/R, INSU/CNRS, UPMC-Paris 6, and by the ANR (ANR-07-BLAN-0124-01). Parts of this work were supported by IPGP multidisciplinary program PARI, and by Paris–IdF region SESAME Grant N°12015908. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript