Biology subjects

Kuypers, M. M. M.

Publications and source records attributed to Kuypers, M. M. M..

3 recordsLinked to original sources

bioRxiv2023

Mechanism of high energy efficiency of carbon fixation by sulfur-oxidizing symbionts revealed by single-cell analyses and metabolic modeling

In chemosynthetic symbioses between marine invertebrates and autotrophic sulfur-oxidizing bacteria the symbionts feed their host by producing organic compounds from CO2 using reduced sulfur compounds as an energy source. One such symbiosis, the gutless marine worm Olavius algarvensis harbors at least five bacterial symbionts of which four have the genetic potential for an autotrophic metabolism. In this study we combined single-cell analyses of CO2 fixation, CO2 release and bulk uptake, with measurements of O2 respiration, sulfur content, and polyhydroxyalkanoate content, as well as mathematical modelling to investigate how energy derived from sulfur oxidation drives carbon fluxes within the symbiosis and between the holobiont and its habitat. We found that under aerobic conditions without external energy sources only the primary symbiont, Ca. Thiosymbion algarvensis, fixed carbon. This symbiont relied on internal sulfur storage for energy production. Our model showed that the apparent efficiency of carbon fixation driven by sulfur oxidation in the symbiosis was higher than thermodynamically feasible if only stored sulfur was considered as source of energy and reducing equivalents. The model and additional calculations showed that reducing equivalents must be derived from a different source than energy. We identified the large amounts of polyhdroxyalkanoate stored by the symbiont as the likely source of reducing equivalents for carbon fixation in the symbiont which boosts the yield of sulfur-driven carbon fixation. The model also showed that heterotrophic carbon fixation by host tissue is not negligible and has to be considered when assessing transfer of carbon from the symbionts to the host.

microbiology↗

bioRxiv2021

Quantification of archaea-driven freshwater nitrification: from single cell to ecosystem level

Deep oligotrophic lakes sustain large archaeal populations of the class Nitrososphaeria in their hypolimnion. They are thought to be the key ammonia oxidizers in these freshwater systems and as such responsible for the rate-limiting step in nitrification. However, the impact that planktonic Nitrososphaeria have on N cycling in lakes is severely understudied and yet to be quantified. Here, we followed this archaeal population in one of Central Europes largest lakes, Lake Constance, over two consecutive years using metagenomics and metatranscriptomics combined with stable isotope-based activity measurements. A single, highly abundant and transcriptionally active freshwater ecotype of Nitrososphaeria dominated the nitrifying community. Phylogenomic analysis of its metagenome-assembled genome showed that this ecotype represents a new lacustrine Nitrosopumilus species. Stable isotope probing revealed that Nitrososphaeria incorporated significantly more 15N-labeled ammonium than most other microorganisms at near-natural conditions and oxidized ammonia at an average rate of 0.22 {+/-} 0.11 fmol cell-1 d-1. This translates to 1.9 gigagram of ammonia oxidized per year, corresponding to 12% of the N-biomass produced annually by photosynthetic organisms in Lake Constance. Here, we show that ammonia-oxidizing archaea play an equally important role in the nitrogen cycle of deep oligotrophic lakes as their counterparts in marine ecosystems.

microbiology↗

bioRxiv2018

Dark aerobic sulfide oxidation by anoxygenic phototrophs in the anoxic waters of Lake Cadagno

SUMMARYAnoxygenic phototrophic sulfide oxidation by green and purple sulfur bacteria (PSB) plays a key role in sulfide removal from anoxic shallow sediments and stratified waters. Although some PSB can also oxidize sulfide with nitrate and oxygen, little is known about the prevalence of this chemolithotrophic lifestyle in the environment. In this study, we investigated the role of these phototrophs in light-independent sulfide removal in the chemocline of Lake Cadagno. Our temporally resolved, high-resolution chemical profiles indicated that dark sulfide oxidation was coupled to high oxygen consumption rates of ~9 M O2{middle dot}h-1. Single-cell analyses of lake water incubated with 13CO2 in the dark revealed that Chr. okenii was to a large extent responsible for aerobic sulfide oxidation and it accounted for up to 40 % of total dark carbon fixation. The genome of Chr. okenii reconstructed from the Lake Cadagno metagenome confirms its capacity for microaerophilic growth and provides further insights into its metabolic capabilities. Moreover, our genomic and single-cell data indicated that other PSB grow microaerobically in these apparently anoxic waters. Altogether, our observations suggest that aerobic respiration may not only play an underappreciated role in anoxic environments, but also that organisms typically considered strict anaerobes may be involved.\n\nORIGINALITY-SIGNIFICANCE STATEMENTThis study reveals that dark aerobic sulfide oxidation within an anoxic layer dominated by anoxygenic phototrophic bacteria in the stratified water column of Lake Cadagno is to a large extent carried out by the anoxygenic phototrophic bacterium Chromatium okenii. Our findings imply that aerobic metabolisms may be more prevalent in anoxic zones than previously thought. We also present an environmental metagenome-assembled genome of Chr. okenii which is the first genome sequence for the genus Chromatium and reveals new interesting physiological features of this environmentally relevant organism, including its capacity for aerobic respiration.

microbiology↗