Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses

Author(s)
Abhishek Srivastava, Daniele De Corte, Juan A L Garcia, Brandon K Swan, Ramunas Stepanauskas, Gerhard J Herndl, Eva Sintes
Abstract

BACKGROUND: Heterotrophic microbes inhabiting the dark ocean largely depend on the settling of organic matter from the sunlit ocean. However, this sinking of organic materials is insufficient to cover their demand for energy and alternative sources such as chemoautotrophy have been proposed. Reduced sulfur compounds, such as thiosulfate, are a potential energy source for both auto- and heterotrophic marine prokaryotes.

METHODS: Seawater samples were collected from Labrador Sea Water (LSW, ~ 2000 m depth) in the North Atlantic and incubated in the dark at in situ temperature unamended, amended with 1 µM thiosulfate, or with 1 µM thiosulfate plus 10 µM glucose and 10 µM acetate (thiosulfate plus dissolved organic matter, DOM). Inorganic carbon fixation was measured in the different treatments and samples for metatranscriptomic analyses were collected after 1 h and 72 h of incubation.

RESULTS: Amendment of LSW with thiosulfate and thiosulfate plus DOM enhanced prokaryotic inorganic carbon fixation. The energy generated via chemoautotrophy and heterotrophy in the amended prokaryotic communities was used for the biosynthesis of glycogen and phospholipids as storage molecules. The addition of thiosulfate stimulated unclassified bacteria, sulfur-oxidizing Deltaproteobacteria (SAR324 cluster bacteria), Epsilonproteobacteria (Sulfurimonas sp.), and Gammaproteobacteria (SUP05 cluster bacteria), whereas, the amendment with thiosulfate plus DOM stimulated typically copiotrophic Gammaproteobacteria (closely related to Vibrio sp. and Pseudoalteromonas sp.).

CONCLUSIONS: The gene expression pattern of thiosulfate utilizing microbes specifically of genes involved in energy production via sulfur oxidation and coupled to CO

2 fixation pathways coincided with the change in the transcriptional profile of the heterotrophic prokaryotic community (genes involved in promoting energy storage), suggesting a fine-tuned metabolic interplay between chemoautotrophic and heterotrophic microbes in the dark ocean. Video Abstract.

Organisation(s)
Functional and Evolutionary Ecology
External organisation(s)
Konrad-Lorenz-Institut für Vergleichende Verhaltensforschung, Carl von Ossietzky Universität Oldenburg, National Oceanography Centre Southampton, Institut La Ferreria, National Biodefense Analysis and Countermeasures Center, Bigelow Laboratory for Ocean Sciences, Royal Netherlands Institute for Sea Research, Centro Oceanográfico de Baleares
Journal
Microbiome
Volume
11
ISSN
2049-2618
DOI
https://doi.org/10.1186/s40168-023-01688-7
Publication date
11-2023
Peer reviewed
Yes
Austrian Fields of Science 2012
106021 Marine biology
Keywords
ASJC Scopus subject areas
Microbiology (medical), Microbiology
Sustainable Development Goals
SDG 14 - Life Below Water
Portal url
https://ucrisportal.univie.ac.at/en/publications/interplay-between-autotrophic-and-heterotrophic-prokaryotic-metabolism-in-the-bathypelagic-realm-revealed-by-metatranscriptomic-analyses(2fa62872-0ef9-4736-99a9-473fa0780054).html