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

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.

Thousands of small, novel genes predicted in global phage genomes

“…Identification of $40,000 small-gene families in phage contigs To predict novel small genes in phages, we first downloaded IMG/ VR (Paez-Espino et al, 2017a;Roux et al, 2021), which contains 2,377,994 viral contigs for a combined total of over 48 billion bases of DNA. This database represents a large collection of viral datasets (Bushman et al, 2019;Espı ´nola et al, 2018;Garcia et al, 2020;Gregory et al, 2019Gregory et al, , 2020Mehrshad et al, 2021;Mobilian et al, 2020;Nayfach et al, 2021a;Paez-Espino et al, 2017b, 2019Roux et al, 2019;Schulz et al, 2020). From these viral contigs, we A B Figure 1.…”

Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

“…5 ). P. aespoeensis was originally isolated from another subsurface location in the Fennoscandian Shield (Äspö, Sweden) [ 86 ], and belongs to the core microbiome of the aquifer in this crystalline rock [ 9 ]. Peptides from the beta subunit of adenylylsulfate reductase (AprB) were also detected in the P. aespoeensis proteome (Fig.…”

“…They are typically slow-growing, with long generation times ranging from months to years [ 2 – 5 ]. Despite their slow growth, they are active [ 6 – 9 ] and can respond to changes in subsurface conditions [ 10 , 11 ]. Understanding the drivers of microbial metabolism in the subsurface is therefore an important consideration for subsurface activities related to energy production, storage, and waste disposal.…”

Genetic diversity in terrestrial subsurface ecosystems impacted by geological degassing

“…On the other hand, the genome structures indicated a faster ability to replicate for organisms in the deep subsurface. This faster possible generation times with depth can be explained by the strategy employed by subsurface microorganisms recently termed as “halt and catch fire” 46 . This strategy refers to an adaptation to nutrient-poor environments like the deep subsurface, where organisms need to adapt to utilize short bursts of available nutrients and thus replicate fast during times when nutrients are available.…”