Nutrient supplementation experiments with saltern microbial communities implicate utilization of DNA as a source of phosphorus

Zhengshuang Hua,Olga Zhaxybayeva,Matthew Ouellette,Andrea M Makkay,R Thane Papke

doi:10.1038/s41396-021-00960-8

Abstract

All environments including hypersaline ones harbor measurable concentrations of dissolved extracellular DNA (eDNA) that can be utilized by microbes as a nutrient. However, it remains poorly understood which eDNA components are used, and who in a community utilizes it. For this study, we incubated a saltern microbial community with combinations of carbon, nitrogen, phosphorus, and DNA, and tracked the community response in each microcosm treatment via 16S rRNA and rpoB gene sequencing. We show that microbial communities used DNA only as a phosphorus source, and provision of other sources of carbon and nitrogen was needed to exhibit a substantial growth. The taxonomic composition of eDNA in the water column changed with the availability of inorganic phosphorus or supplied DNA, hinting at preferential uptake of eDNA from specific organismal sources. Especially favored for growth was eDNA from the most abundant taxa, suggesting some haloarchaea prefer eDNA from closely related taxa. The preferential eDNA consumption and differential growth under various nutrient availability regimes were associated with substantial shifts in the taxonomic composition and diversity of microcosm communities. Therefore, we conjecture that in salterns the microbial community assembly is driven by the available resources, including eDNA.

Highlights

The observed patterns of microbial community growth under different treatments are consistent with the consumed amounts of C, N, and Pi, as measured by comparing the total organic carbon (TOC), total nitrogen (TN), and total phosphorus (TP) in the filtered untreated water samples and in the treated filtered water samples after the communities reached the stationary phase
We propose that the availability of Hfx. volcanii DNA and inorganic phosphorus in slow- and fast-growing communities, respectively, results in the reduced uptake of available extracellular DNA (eDNA) as a P source, leading to eDNA accumulation in the environment and causing the observed changes in eDNA operational taxonomic units (OTUs) composition
From comparisons of slow-growing microcosms with and without added Hfx. volcanii DNA, we found that when Hfx. volcanii DNA is not provided, eDNA from five Halorubraceae and Haloarculaceae abundant haloarchaeal OTUs (ahOTUs) is depleted and eDNA of 305 additional OTUs become undetectable in the water columns (Supplementary Table S8)

Summary

Introduction

Dissolved extracellular DNA (eDNA) in the environment plays important roles in global cycles of carbon (C), nitrogen (N), and phosphorus (P). It is found at measurable concentrations in every analyzed habitat [1,2,3,4] and is estimated to amount to gigatons globally [5]. EDNA becomes available for resident organisms to utilize, and in some environments eDNA turnover rates can be as short as a few hours [12]. Seasonal variability and type of habitat can increase the residence time of eDNA to months and years [13, 14], despite the presence and high activity of secreted extracellular nucleases [3]. Adsorption to minerals and particles can make eDNA unavailable for microorganisms [15], but factors like nutrient obtainability, and the presence of salt could contribute to the stability, availability and utilization of the available eDNA [13, 16]

Methods

Results

Conclusion