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

Maliheh Mehrshad,Emma Bell,Domenico Simone,Moritz Buck,Margarita Lopez-Fernandez,Rizlan Bernier-Latmani,Stefan Bertilsson,John Sundh,Mark Dopson

doi:10.1038/s41467-021-24549-z

Abstract

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.

Highlights

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
The Äspö Hard Rock Laboratory (HRL) and Olkiluoto drillholes were sampled over time, covering a diversity of aquifers representing waters of differing ages and both planktonic and biofilm-associated communities
In order to provide a genome-resolved view of the Fennoscandian Shield bedrock Archaeal and bacterial communities, collected samples were used for an integrated analysis by combining metagenomes (n = 44), single-cell genomes (n = 564), and metatranscriptomes (n = 9)

Summary

Introduction

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. By augmenting this dataset with 564 sequenced single-cell amplified genomes (SAGs; 114 of which were ≥ 50% complete with ≤ 5% contamination), we present a comprehensive genomic database for the archaeal and bacterial diversity of these oligotrophic deep groundwaters, hereafter referred to as the Fennoscandian Shield genomic database (FSGD; statistics in Fig. 1A & Supplementary Data 2).

Results

Conclusion