Dynamic cellular complexity of anoxygenic phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno.

Francesco Danza,Nicola Storelli,Samuele Roman,Mauro Tonolla,Samuel Lüdin,Inês A Cardoso Pereira

doi:10.1371/journal.pone.0189510

Abstract

The meromictic Lake Cadagno is characterized by a compact chemocline with high concentrations of anoxygenic phototrophic purple sulfur bacteria (PSB) and green sulfur bacteria (GSB). The co-occurrence of phylogenetically distant bacterial groups such as PSB and GSB in the same ecological niche, makes the chemocline of Lake Cadagno an ideal system for studying the conditions and consequences of coexistence of photosynthetic bacteria populations. In this study, we applied flow cytometry (FCM) as a fast tool to identify metabolic changes due to the production and consumption of inclusion bodies such as sulfur globules (SGBs), and follow population dynamics of closely related anoxygenic photosynthetic sulfur bacteria in their natural environment. Large-celled PSB Chromatium okenii and GSB Chlorobium populations were reliably separated and identified due to differences in auto-fluorescence and cell size. Moreover, we showed that these dominant taxa share the same ecological niche over seasonal periods. Taking advantage of FCM detection of dynamic cellular complexity variation during phases of photosynthetic activity, we identified an unexpected alternation in PSB versus GSB metabolic activity, indicating dynamic interspecific interactions between these two populations.

Highlights

Photosynthesis converts light energy to chemical energy stored in the form of organic carbon compounds through the fixation of inorganic CO2
The amount of sulfur globules (SGB) in large-celled purple sulfur bacteria (PSB) C. okenii decreased over time under continuous light irradiation in microcosm without addition of extra sulfide (Fig 1)
Under irradiation the H2S-oxidation rate of PSB C. okenii correlated with variations in sideward scatter (SSC) signal intensity and number of intracellular SGBs (Fig 2A)

Summary

Introduction

Photosynthesis converts light energy to chemical energy stored in the form of organic carbon compounds through the fixation of inorganic CO2. This process enables autotrophic organisms to form the basis of food webs in most ecosystems as primary producers. Global estimates suggest that bacteria are responsible for up to 98% of organic carbon produced on Earth [1], but they are key mediators in most other biogeochemical cycles [2]. Other than oxygenic photosynthesis occurring in plants, algae and aerobic microorganisms, anoxygenic photosynthesis is an important ecosystem process driven by anaerobic photosynthetic. Coexistence of anoxygenic phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno microorganisms, which play a dominant role in CO2-fixation in anaerobic environments [3,4]. In contrast to water photolysis as electron source, anoxygenic photosynthesis uses electron donors such as hydrogen (H2), hydrogen sulfide (HS-), thiosulfate (S2O32-), sulfur (S0) and reduced iron (Fe2+)

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Discussion

Conclusion