Microbial Processes and Microbial Communities in the Water Column of the Polar Meromictic Lake Bol'shie Khruslomeny at the White Sea Coast.

Alexander S Savvichev,Elena F Veslopolova,Igor I Rusanov,Nikolai V Ravin,Galina N Losyuk,Vitaly V Kadnikov,Elena D Krasnova,Nataliya M Kokryatskaya,Nikolai A Demidenko,Anna Yu Kallistova,Elena E Zakharova,Andrey V Mardanov,Dmitry A Voronov,Alexey V Beletsky,Pavel A Sigalevich,Nikolai A Belyaev,Nikolay V Pimenov

doi:10.3389/fmicb.2020.01945

Abstract

Microbiological, molecular ecological, biogeochemical, and isotope geochemical research was carried out at the polar Lake Bol’shie Khruslomeny at the coast of the Kandalaksha Bay, White Sea in March and September 2017. The uppermost mixolimnion was oxic, with low salinity (3–5%). The lower chemocline layer was brown-green colored, with very high content of particulate organic matter (up to 11.8 mg C L–1). The lowermost monimolimnion had marine salinity (22–24%) and very high concentrations of sulfide (up to 18 mmol L–1) and CH4 (up to 1.8 mmol L–1). In the chemocline, total microbial abundance and the rate of anoxygenic photosynthesis were 8.8 × 106 cells mL–1 and 34.4 μmol C L–1 day–1, respectively. Both in March and September, sulfate reduction rate increased with depth, peaking (up to 0.6–1.1 μmol S L–1 day–1) in the lower chemocline. Methane oxidation rates in the chemocline were up to 85 and 180 nmol CH4 L–1 day–1 in March and September, respectively; stimulation of this process by light was observed in September. The percentages of cyanobacteria and methanotrophs in the layer where light-induced methane oxidation occurred were similar, ∼2.5% of the microbial community. Light did not stimulate methane oxidation in deeper layers. The carbon isotope composition of particulate organic matter (δ13C-Corg), dissolved carbonates (δ13C-DIC), and methane (δ13C- CH4) indicated high microbial activity in the chemocline. Analysis of the 16S rRNA gene sequences revealed predominance of Cyanobium cyanobacteria (order Synechococcales) in the mixolimnion. Green sulfur bacteria Chlorobium phaeovibrioides capable of anoxygenic photosynthesis constituted ∼20% of the chemocline community both in March and in September. Methyloprofundus gammaptoteobacteria (family Methylomonaceae) were present in the upper chemocline, where active methane oxidation occurred. During winter, cyanobacteria were less abundant in the chemocline, while methanotrophs occurred in higher horizons, including the under-ice layer. Chemolithotrophic gammaproteobacteria of the genus Thiomicrorhabdus, oxidizing reduced sulfur compounds at low oxygen concentrations, were revealed in the chemocline in March. Both in March and September archaea constituted up to 50% of all microorganisms in the hypolimnion. The percentage of putative methanogens in the archaeal community was low, and they occurred mainly in near-bottom horizons.

Highlights

Meromictic lakes are formations in which microbial geochemical activity is most pronounced (Overmann et al, 1991; Crowe et al, 2014; Walter et al, 2014)
Since microbial communities developing in the chemocline of meromictic lakes carry out geochemically important redox processes, such basins are of interest to microbiologists
Two layers of photosynthetic activity are present in meromictic lakes: the layer of oxygenic photosynthesis in the surface or subsurface horizon and the layer of anoxygenic photosynthesis, which usually coincides with the chemocline and is one to several meters thick

Summary

Introduction

Meromictic (permanently stratified) lakes are formations in which microbial geochemical activity is most pronounced (Overmann et al, 1991; Crowe et al, 2014; Walter et al, 2014). The highest rates of microbial processes occur in the zone where oxic and anoxic (euxinic, oxygen-free, sulfide-enriched) water layers contact. This zone is termed a chemocline (Overmann et al, 1991), pycnocline (Galand et al, 2012), a transitory zone (Schmidtova et al, 2009), or an oxic–anoxic interface (Vetriani et al, 2003). Among the natural compounds acting as oxidizers, oxygen is the most energetically advantageous electron acceptor for heterotrophic organisms consuming organic matter (Wang and Van Cappellen, 1996). Microorganisms oxidize reduced sulfur, iron, and manganese compounds (Canfield et al, 1993), as well as methane (Eller et al, 2005), primarily using oxygen. The processes occurring at micromolar oxygen concentrations have not been studied until recently (Brand et al, 2016)

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