Energy efficiency and biological interactions define the core microbiome of deep oligotrophic groundwater

While oligotrophic deep groundwaters host active microbes attuned to the low-end of the bioenergetics spectrum, the ecological constraints on microbial niches in these ecosystems and their consequences for microbiome convergence are unknown. Here, we provide a genome-resolved, integrated omics analysis comparing archaeal and bacterial communities in disconnected fracture fluids of the Fennoscandian Shield in Europe. Leveraging a dataset that combines metagenomes, single cell genomes, and metatranscriptomes, we show that groundwaters flowing in similar lithologies offer fixed niches that are occupied by a common core microbiome. Functional expression analysis highlights that these deep groundwater ecosystems foster diverse, yet cooperative communities adapted to this setting. We suggest that these communities stimulate cooperation by expression of functions related to ecological traits, such as aggregate or biofilm formation, while alleviating the burden on microorganisms producing compounds or functions that provide a collective benefit by facilitating reciprocal promiscuous metabolic partnerships with other members of the community. We hypothesize that an episodic lifestyle enabled by reversible bacteriostatic functions ensures the subsistence of the oligotrophic deep groundwater microbiome. Ecological constraints on microbial niches in oligotrophic deep groundwaters remain elusive. This study provides support for the existence of a common core microbiome in two deep groundwater biomes of the Fennoscandian Shield using a genome-resolved, integrated omics analysis.

Active sulfur cycling in the terrestrial deep subsurface

Emma Bell, Rizlan Bernier-Latmani, Manon Frutschi

The deep terrestrial subsurface remains an environment where there is limited understanding of the extant microbial metabolisms. At Olkiluoto, Finland, a deep geological repository is under construction for the final storage of spent nuclear fuel. It is therefore critical to evaluate the potential impact microbial metabolism, including sulfide generation, could have upon the safety of the repository. We investigated a deep groundwater where sulfate is present, but groundwater geochemistry suggests limited microbial sulfate-reducing activity. Examination of the microbial community at the genome-level revealed microorganisms with the metabolic capacity for both oxidative and reductive sulfur transformations. Deltaproteobacteria are shown to have the genetic capacity for sulfate reduction and possibly sulfur disproportionation, while Rhizobiaceae, Rhodocyclaceae, Sideroxydans, and Sulfurimonas oxidize reduced sulfur compounds. Further examination of the proteome confirmed an active sulfur cycle, serving for microbial energy generation and growth. Our results reveal that this sulfide-poor groundwater harbors an active microbial community of sulfate-reducing and sulfide-oxidizing bacteria, together mediating a sulfur cycle that remained undetected by geochemical monitoring alone. The ability of sulfide-oxidizing bacteria to limit the accumulation of sulfide was further demonstrated in groundwater incubations and highlights a potential sink for sulfide that could be beneficial for geological repository safety.

2020

Optimised biomolecular extraction for metagenomic analysis of microbial biofilms from high-mountain streams

Tom Ian Battin, Jade Brandani, Susheel Bhanu Busi, Stylianos Fodelianakis, Hannes Markus Peter, Paraskevi Pramateftaki

Glacier-fed streams (GFS) are harsh ecosystems dominated by microbial life organized in benthic biofilms, yet the biodiversity and ecosystem functions provided by these communities remain under-appreciated. To better understand the microbial processes and communities contributing to GFS ecosystems, it is necessary to leverage high throughput sequencing. Low biomass and high inorganic particle load in GFS sediment samples may affect nucleic acid extraction efficiency using extraction methods tailored to other extreme environments such as deep-sea sediments. Here, we benchmarked the utility and efficacy of four extraction protocols, including an up-scaled phenolchloroform protocol. We found that established protocols for comparable sample types consistently failed to yield sufficient high-quality DNA, delineating the extreme character of GFS. The methods differed in the success of downstream applications such as library preparation and sequencing. An adapted phenol-chloroform-based extraction method resulted in higher yields and better recovered the expected taxonomic profile and abundance of reconstructed genomes when compared to commercially-available methods. Affordable and straight-forward, this method consistently recapitulated the abundance and genomes of a mock community, including eukaryotes. Moreover, by increasing the amount of input sediment, the protocol is readily adjustable to the microbial load of the processed samples without compromising protocol efficiency. Our study provides a first systematic and extensive analysis of the different options for extraction of nucleic acids from glacier-fed streams for high-throughput sequencing applications, which may be applied to other extreme environments.

PEERJ INC2020

The architecture of benthic biofilms - Linking hydraulics to spatially structured processes

Anna Depetris

Biofilms are spatially structured ecosystems, characterized by patterns and architectural features determined by the interplay between endogenous and exogenous processes. As in many other structured ecosystems, the characterization of spatial interactions is pivotal to infer ecological functions. To date, the majority of studies have focused on pattern formation and morphology of single-species biofilm in microfluidics devices, drawing important conclusions about the physiological mechanisms mediating this phenomenon. However, the study of spatial organization of multi-species biofilms growing under conditions that resemble the native habitat has not been conducted extensively yet. The aim of this PhD thesis is the systematic investigation of spatial patterns formation in freshwater phototrophic benthic biofilms, under quasi-natural conditions. Benthic biofilms are a type of microbial community of global importance, for instance, for carbon cycling within streams. They are characterized by close metabolic interactions between autotrophic and heterotrophic microorganisms, and they are tightly shaped by the hydrodynamics of the surrounding water. We will research the formation of spatial organization in benthic biofilms with a special focus on the link between hydrodynamics, biofilm architecture, metabolism and biodiversity. We expect that this comprehensive view will permit an enhanced mechanistic understanding of the emergence of spatial organization in phototrophic benthic biofilms, as well as its ecological consequences.

EPFL2021