Cédric Morana

Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin

Iron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth’s early history. Before the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled Earth’s early biosphere providing energy to drive microbial growth and evolution over billions of years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving models for early biological production untested and imperative ecological context for the evolution of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth’s largest sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

Carbon Cycling of Lake Kivu (East Africa): Net Autotrophy in the Epilimnion and Emission of CO2 to the Atmosphere Sustained by Geogenic Inputs

We report organic and inorganic carbon distributions and fluxes in a large (>2000 km2) oligotrophic, tropical lake (Lake Kivu, East Africa), acquired during four field surveys, that captured the seasonal variations (March 2007–mid rainy season, September 2007–late dry season, June 2008–early dry season, and April 2009–late rainy season). The partial pressure of CO2 (pCO2) in surface waters of the main basin of Lake Kivu showed modest spatial (coefficient of variation between 3% and 6%), and seasonal variations with an amplitude of 163 ppm (between 579±23 ppm on average in March 2007 and 742±28 ppm on average in September 2007). The most prominent spatial feature of the pCO2 distribution was the very high pCO2 values in Kabuno Bay (a small sub-basin with little connection to the main lake) ranging between 11213 ppm and 14213 ppm (between 18 and 26 times higher than in the main basin). Surface waters of the main basin of Lake Kivu were a net source of CO2 to the atmosphere at an average rate of 10.8 mmol m−2 d−1, which is lower than the global average reported for freshwater, saline, and volcanic lakes. In Kabuno Bay, the CO2 emission to the atmosphere was on average 500.7 mmol m−2 d−1 (∼46 times higher than in the main basin). Based on whole-lake mass balance of dissolved inorganic carbon (DIC) bulk concentrations and of its stable carbon isotope composition, we show that the epilimnion of Lake Kivu was net autotrophic. This is due to the modest river inputs of organic carbon owing to the small ratio of catchment area to lake surface area (2.15). The carbon budget implies that the CO2 emission to the atmosphere must be sustained by DIC inputs of geogenic origin from deep geothermal springs.

Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu

The microbial community composition in meromictic Lake Kivu, with one of the largest CH4 reservoirs, was studied using 16S rDNA and ribosomal RNA (rRNA) pyrosequencing during the dry and rainy seasons. Highly abundant taxa were shared in a high percentage between bulk (DNA-based) and active (RNA-based) bacterial communities, whereas a high proportion of rare species was detected only in either an active or bulk community, indicating the existence of a potentially active rare biosphere and the possible underestimation of diversity detected when using only one nucleic acid pool. Most taxa identified as generalists were abundant, and those identified as specialists were more likely to be rare in the bulk community. The overall number of environmental parameters that could explain the variation was higher for abundant taxa in comparison to rare taxa. Clustering analysis based on operational taxonomic units (OTUs at 0.03 cutoff) level revealed significant and systematic microbial community composition shifts with depth. In the oxic zone, Actinobacteria were found highly dominant in the bulk community but not in the metabolically active community. In the oxic–anoxic transition zone, highly abundant potentially active Nitrospira and Methylococcales were observed. The co-occurrence of potentially active sulfur-oxidizing and sulfate-reducing bacteria in the anoxic zone may suggest the presence of an active yet cryptic sulfur cycle.

Variability of Carbon Dioxide and Methane in the Epilimnion of Lake Kivu

We report a dataset of the partial pressure of CO2 (pCO2) and methane concentrations (CH4) in the surface waters of Lake Kivu obtained during four cruises covering the two main seasons (rainy and dry). Spatial gradients of surface pCO2 and CH4 concentrations were modest in the main basin. In Kabuno Bay, pCO2 and CH4 concentrations in surface waters were higher, owing to the stronger influence of subaquatic springs from depth. Seasonal variations of pCO2 and CH4 in the main basin of Lake Kivu were strongly driven by deepening of the epilimnion and the resulting entrainment of water characterized by higher pCO2 and CH4 concentrations. Physical and chemical vertical patterns in Kabuno Bay were seasonally stable, owing to a stronger stratification and smaller surface area inducing fetch limitation of wind driven turbulence. A global and regional cross-system comparison of pCO2 and CH4 concentrations in surface waters of lakes highlights the peculiarity of Kabuno Bay in terms of pCO2 values in surface waters. In terms of surface CH4 concentrations, both Kabuno Bay and the main basin of Lake Kivu are at the lower end of values in lakes globally, despite the huge amounts of CH4 and CO2 in the deeper layers of the lake.

Bacterioplankton niche partitioning in the use of phytoplankton-derived dissolved organic carbon: quantity is more important than quality

Some prokaryotes are known to be specialized in the use of phytoplankton-derived dissolved organic carbon (DOCp) originated by exudation or cell lysis; however, direct quantification measurements are extremely rare. Several studies have described bacterial selectivity based on DOCp quality, but very few have focused on the quantity of DOCp, and the relative importance of each of these variables (for example, quantity versus quality) on prokaryote responses. We applied an adapted version of the MAR-FISH (microautoradiography coupled with catalyzed reporter deposition fluorescence in situ hybridization) protocol using radiolabelled exudates from axenic algal cultures to calculate a specialization index (d’) for large bacterioplankton phylogenetic groups using DOCp from different phytoplankton species and at different concentrations to elucidate to what extent the bacterial response to DOCp is driven by resource quantity (different DOCp concentrations) or by quality (DOCp from different phytoplankton species). All bacterial phylogenetic groups studied had lower d’ at higher DOCp concentration, indicating more generalist behavior at higher resource availabilities. Indeed, at increasing resource concentrations, most bacterial groups incorporated DOCp indiscriminately, regardless of its origin (or quality). At low resource concentrations, only some specialists were able to actively incorporate the various types of organic matter effectively. The variability of bacterial responses to different treatments was systematically higher at varying concentrations than at varying DOCp types, suggesting that, at least for this range of concentrations (10–100 μM), DOCp quantity affects bacterial responses more than quality does. Therefore, resource quantity may be more relevant than resource quality in the bacterial responses to DOCp and affect how bacterioplankton use phytoplankton-derived carbon.

Microbial Ecology of Lake Kivu

We review available data on archaea, bacteria and small eukaryotes in an attempt to provide a general picture of microbial diversity, abundances and microbe-driven processes in Lake Kivu surface and intermediate waters (ca. 0–100 m). The various water layers present contrasting physical and chemical properties and harbour very different microbial communities supported by the vertical redox structure. For instance, we found a clear vertical segregation of archaeal and bacterial assemblages between the oxic and the anoxic zone of the surface waters. The presence of specific bacterial (e.g. Green Sulfur Bacteria) and archaeal (e.g. ammonia-oxidising archaea) communities and the prevailing physico-chemical conditions point towards the redoxcline as the most active and metabolically diverse water layer. The archaeal assemblage in the surface and intermediate water column layers was mainly composed by the phylum Crenarchaeota, by the recently defined phylum Thaumarchaeota and by the phylum Euryarchaeota. In turn, the bacterial assemblage comprised mainly ubiquitous members of planktonic assemblages of freshwater environments (Actinobacteria, Bacteroidetes and Betaproteobacteria among others) and other less commonly retrieved phyla (e.g. Chlorobi, Clostridium and Deltaproteobacteria). The community of small eukaryotes (<5 μm) mainly comprised Stramenopiles, Alveolata, Cryptophyta, Chytridiomycota, Kinetoplastea and Choanoflagellida, by decreasing order of richness. The total prokaryotic abundance ranged between 0.5 × 106 and 2.0 × 106 cells mL−1, with maxima located in the 0–20 m layer, while phycoerythrin-rich Synechococcus-like picocyanobacteria populations were comprised between 0.5 × 105 and 2.0 × 105 cells mL−1 in the same surface layer. Brown-coloured species of Green Sulfur Bacteria permanently developed at 11m depth in Kabuno Bay and sporadically in the anoxic waters of the lower mixolimnion of the main basin. The mean bacterial production was estimated to 336 mg C m−2 day−1. First estimates of the re-assimilation by bacterioplankton of dissolved organic matter excreted by phytoplankton showed high values of dissolved primary production (ca. 50% of total production). The bacterial carbon demand can totally be fuelled by phytoplankton production. Overall, recent studies have revealed a high microbial diversity in Lake Kivu, and point towards a central role of microbes in the biogeochemical and ecological functioning of the surface layers, comprising the mixolimnion and the upper chemocline.