Resource partitioning and amino acid assimilation in a terrestrial geothermal spring

Abstract

High-temperature geothermal springs host simplified microbial communities; however, the activities of individual microorganisms and their roles in the carbon cycle in nature are not well understood. Here, quantitative stable isotope probing (qSIP) was used to track the assimilation of 13C-acetate and 13C-aspartate into DNA in 74 °C sediments in Gongxiaoshe Hot Spring, Tengchong, China. This revealed a community-wide preference for aspartate and a tight coupling between aspartate incorporation into DNA and the proliferation of aspartate utilizers during labeling. Both 13C incorporation into DNA and changes in the abundance of taxa during incubations indicated strong resource partitioning and a significant phylogenetic signal for aspartate incorporation. Of the active amplicon sequence variants (ASVs) identified by qSIP, most could be matched with genomes from Gongxiaoshe Hot Spring or nearby springs with an average nucleotide similarity of 99.4%. Genomes corresponding to aspartate primary utilizers were smaller, near-universally encoded polar amino acid ABC transporters, and had codon preferences indicative of faster growth rates. The most active ASVs assimilating both substrates were not abundant, suggesting an important role for the rare biosphere in the community response to organic carbon addition. The broad incorporation of aspartate into DNA over acetate by the hot spring community may reflect dynamic cycling of cell lysis products in situ or substrates delivered during monsoon rains and may reflect N limitation.

Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes

“…Acetate is a prevalent electron donor and carbon source in both oxic and anoxic environments, and species-specific uptake of acetate was recently studied in a Tengchong spring 44 . Furthermore, acetate oxidation with low potential electron acceptors, such as partially oxidized sulfur compounds, can be an important intersection of the carbon cycle and other element cycles 45 .…”

Quantifying genome-specific carbon fixation in a 750-meter deep subsurface hydrothermal microbial community

“…S1 , Supporting Information ). The relation between DIC, DOC, and primary production in hydrothermal fluids is poorly understood, as are the rates of primary production and DOC production in hydrothermal systems (Le Bris et al 2019 , Lai et al 2023 ). Thus, we investigated the effect of DIC concentration on microbial carbon fixation in alkaline subsurface hydrothermal fluids from deep subsurface (750-m) fluids from one of the sampling locations in the Bardakçılar geothermal field (Fig.…”

“…Specifically, quantitative DNA stable isotope probing (qSIP) uses labeled carbon ( 13 C) substrates to quantify the amount of carbon assimilated by all detectable microbial taxa in an environmental sample (Hungate et al 2015 ). The qSIP methodology with 13 C-labeled substrates has been applied to broad range of environments such as soil (Hungate et al 2015 , Morrissey et al 2016 , Starr et al 2021 ), marine sediments (Orsi et al 2020 ), seawater (Orsi et al 2021 ), ocean crust (Coskun et al 2022 ), and geothermal terrestrial springs (Lai et al 2023 ). Here, we performed qSIP experiments by adding the H 13 CO 3 − at three different concentrations (1, 5, and 10 mM) to test the effect of naturally available range of bicarbonate concentrations that the microbial communities are exposed to as they are transported through the subsurface aquifer (from 1 to 11 mM; Fig.…”

“…S7 , Supporting Information ). Many of these taxa including the Aquificae are often found in deep subsurface or hydrothermal habitats (Henry et al 1994 , Takai et al 2003 , Hügler et al 2007 , Schubotz et al 2015 , Fullerton et al 2021 , Lai et al 2023 ). The carbon-fixing community at 10 mM bicarbonate concentration was significantly different compared to those in 1 and 5 mM [analysis of similarity (ANOSIM) of 1 and 10 mM: R 2 = 0.676, P = .0045; ANOSIM of 5 and 10 mM: R 2 = 0.906, P = .0021; Fig.…”

“…S9 , Supporting Information ), these results indicate Aquificae MAGs were fixing 13 C-bicarbonate via autotrophy and the rTCA cycle, which is a wide-spread trait in the thermophilic Aquificae (Hügler et al 2007 , Hügler and Sievert 2011 , Gupta 2014 ). Some Aquificae have exhibited mixotrophic metabolism in SIP experiments from hydrothermal springs, via 13 C-labeling from organic sources such as glucose (Schubotz et al 2015 ) and amino acids (Lai et al 2023 ). However, the lack of genes encoding transport proteins for sugars or amino acids in the Aquificae MAGs reported here indicate that the Aquificae taxa inhabiting the alkaline hydrothermal fluids of the 750-m borehole lack this capacity.…”