Abstract

Pelagic aggregates function as biological carbon pumps for transporting fixed organic carbon to sediments. In iron-rich (ferruginous) lakes, photoferrotrophic and chemolithoautotrophic bacteria contribute to CO2 fixation by oxidizing reduced iron, leading to the formation of iron-rich pelagic aggregates (iron snow). The significance of iron oxidizers in carbon fixation, their general role in iron snow functioning and the flow of carbon within iron snow is still unclear. Here, we combined a two-year metatranscriptome analysis of iron snow collected from an acidic lake with protein-based stable isotope probing to determine general metabolic activities and to trace 13CO2 incorporation in iron snow over time under oxic and anoxic conditions. mRNA-derived metatranscriptome of iron snow identified four key players (Leptospirillum, Ferrovum, Acidithrix, Acidiphilium) with relative abundances (59.6–85.7%) encoding ecologically relevant pathways, including carbon fixation and polysaccharide biosynthesis. No transcriptional activity for carbon fixation from archaea or eukaryotes was detected. 13CO2 incorporation studies identified active chemolithoautotroph Ferrovum under both conditions. Only 1.0–5.3% relative 13C abundances were found in heterotrophic Acidiphilium and Acidocella under oxic conditions. These data show that iron oxidizers play an important role in CO2 fixation, but the majority of fixed C will be directly transported to the sediment without feeding heterotrophs in the water column in acidic ferruginous lakes.

Highlights

  • Pelagic aggregates, formed in the water column of lakes and oceans through adsorption of inorganic and organic matter (OM), are composed of microorganisms, phytoplankton, feces, detritus and biominerals [1,2]

  • Marine pelagic aggregates drive the biological carbon pump via the export of photosynthetically derived particulate organic carbon (POC) from the photic zone of the ocean to the deep aphotic zones, where carbon can be sequestered for years before reaching the sediment [4,5,6]

  • Our molecular data consistently show the dominance of autotrophic Fe(II)-oxidizing bacteria (FeOB) (Leptospirillum and Ferrovum) in iron snow, whereas autotrophic communities in marine or lake snow are dominated by phytoplankton

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Summary

Introduction

Pelagic aggregates, formed in the water column of lakes and oceans through adsorption of inorganic and organic matter (OM), are composed of microorganisms, phytoplankton, feces, detritus and biominerals [1,2]. These snow-like aggregates are usually larger than 500 μm and are held together by extracellular polymeric substances (EPS) [3]. In iron-rich ferruginous meromictic lakes, iron-rich pelagic aggregates (iron snow) are formed and dominated by an Fe(III)-rich fraction of more than 35%, rather than OM, Microorganisms 2021, 9, 1368. Low productivity in surface water allows sunlight to penetrate to the chemocline, stimulating anoxygenic phototrophic

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