Key Role of Alphaproteobacteria and Cyanobacteria in the Formation of Stromatolites of Lake Dziani Dzaha (Mayotte, Western Indian Ocean).

Lake Dziani Dzaha is a thalassohaline tropical crater lake located on the "Petite Terre" Island of Mayotte (Comoros archipelago, Western Indian Ocean). Stromatolites are actively growing in the shallow waters of the lake shores. These stromatolites are mainly composed of aragonite with lesser proportions of hydromagnesite, calcite, dolomite, and phyllosilicates. They are morphologically and texturally diverse ranging from tabular covered by a cauliflower-like crust to columnar ones with a smooth surface. High-throughput sequencing of bacterial and archaeal 16S rRNA genes combined with confocal laser scanning microscopy (CLSM) analysis revealed that the microbial composition of the mats associated with the stromatolites was clearly distinct from that of the Arthrospira-dominated lake water. Unicellular-colonial Cyanobacteria belonging to the Xenococcus genus of the Pleurocapsales order were detected in the cauliflower crust mats, whereas filamentous Cyanobacteria belonging to the Leptolyngbya genus were found in the smooth surface mats. Observations using CLSM, scanning electron microscopy (SEM) and Raman spectroscopy indicated that the cauliflower texture consists of laminations of aragonite, magnesium-silicate phase and hydromagnesite. The associated microbial mat, as confirmed by laser microdissection and whole-genome amplification (WGA), is composed of Pleurocapsales coated by abundant filamentous and coccoid Alphaproteobacteria. These phototrophic Alphaproteobacteria promote the precipitation of aragonite in which they become incrusted. In contrast, the Pleurocapsales are not calcifying but instead accumulate silicon and magnesium in their sheaths, which may be responsible for the formation of the Mg-silicate phase found in the cauliflower crust. We therefore propose that Pleurocapsales and Alphaproteobacteria are involved in the formation of two distinct mineral phases present in the cauliflower texture: Mg-silicate and aragonite, respectively. These results point out the role of phototrophic Alphaproteobacteria in the formation of stromatolites, which may open new perspective for the analysis of the fossil record.

Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids From the Laguna Negra Lake (Argentina).

Stromatolites are organo-sedimentary structures that represent some of the oldest records of the early biosphere on Earth. Cyanobacteria are considered as a main component of the microbial mats that are supposed to produce stromatolite-like structures. Understanding the role of cyanobacteria and associated microorganisms on the mineralization processes is critical to better understand what can be preserved in the laminated structure of stromatolites. Laguna Negra (Catamarca, Argentina), a high-altitude hypersaline lake where stromatolites are currently formed, is considered as an analog environment of early Earth. This study aimed at characterizing carbonate precipitation within microbial mats and associated oncoids in Laguna Negra. In particular, we focused on carbonated black pustular mats. By combining Confocal Laser Scanning Microscopy, Scanning Electron Microscopy, Laser Microdissection and Whole Genome Amplification, Cloning and Sanger sequencing, and Focused Ion Beam milling for Transmission Electron Microscopy, we showed that carbonate precipitation did not directly initiate on the sheaths of cyanobacterial Rivularia, which dominate in the mat. It occurred via organo-mineralization processes within a large EPS matrix excreted by the diverse microbial consortium associated with Rivularia where diatoms and anoxygenic phototrophic bacteria were particularly abundant. By structuring a large microbial consortium, Rivularia should then favor the formation of organic-rich laminations of carbonates that can be preserved in stromatolites. By using Fourier Transform Infrared spectroscopy and Synchrotron-based deep UV fluorescence imaging, we compared laminations rich in structures resembling Rivularia to putatively chemically-precipitated laminations in oncoids associated with the mats. We showed that they presented a different mineralogy jointly with a higher content in organic remnants, hence providing some criteria of biogenicity to be searched for in the fossil record.

High reactivity of deep biota under anthropogenic CO2 injection into basalt.

Basalts are recognized as one of the major habitats on Earth, harboring diverse and active microbial populations. Inconsistently, this living component is rarely considered in engineering operations carried out in these environments. This includes carbon capture and storage (CCS) technologies that seek to offset anthropogenic CO2 emissions into the atmosphere by burying this greenhouse gas in the subsurface. Here, we show that deep ecosystems respond quickly to field operations associated with CO2 injections based on a microbiological survey of a basaltic CCS site. Acidic CO2-charged groundwater results in a marked decrease (by ~ 2.5-4) in microbial richness despite observable blooms of lithoautotrophic iron-oxidizing Betaproteobacteria and degraders of aromatic compounds, which hence impact the aquifer redox state and the carbon fate. Host-basalt dissolution releases nutrients and energy sources, which sustain the growth of autotrophic and heterotrophic species whose activities may have consequences on mineral storage.

Mineralizing Filamentous Bacteria from the Prony Bay Hydrothermal Field Give New Insights into the Functioning of Serpentinization-Based Subseafloor Ecosystems.

Despite their potential importance as analogs of primitive microbial metabolisms, the knowledge of the structure and functioning of the deep ecosystems associated with serpentinizing environments is hampered by the lack of accessibility to relevant systems. These hyperalkaline environments are depleted in dissolved inorganic carbon (DIC), making the carbon sources and assimilation pathways in the associated ecosystems highly enigmatic. The Prony Bay Hydrothermal Field (PHF) is an active serpentinization site where, similar to Lost City (Mid-Atlantic Ridge), high-pH fluids rich in H2 and CH4 are discharged from carbonate chimneys at the seafloor, but in a shallower lagoonal environment. This study aimed to characterize the subsurface microbial ecology of this environment by focusing on the earliest stages of chimney construction, dominated by the discharge of hydrothermal fluids of subseafloor origin. By jointly examining the mineralogy and the microbial diversity of the conduits of juvenile edifices at the micrometric scale, we find a central role of uncultivated bacteria belonging to the Firmicutes in the ecology of the PHF. These bacteria, along with members of the phyla Acetothermia and Omnitrophica, are identified as the first chimneys inhabitants before archaeal Methanosarcinales. They are involved in the construction and early consolidation of the carbonate structures via organomineralization processes. Their predominance in the most juvenile and nascent hydrothermal chimneys, and their affiliation with environmental subsurface microorganisms, indicate that they are likely discharged with hydrothermal fluids from the subseafloor. They may thus be representative of endolithic serpentinization-based ecosystems, in an environment where DIC is limited. In contrast, heterotrophic and fermentative microorganisms may consume organic compounds from the abiotic by-products of serpentinization processes and/or from life in the deeper subsurface. We thus propose that the Firmicutes identified at PHF may have a versatile metabolism with the capability to use diverse organic compounds from biological or abiotic origin. From that perspective, this study sheds new light on the structure of deep microbial communities living at the energetic edge in serpentinites and may provide an alternative model of the earliest metabolisms.