Degradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments

Sherlynette Pérez Castro,Kathleen Regan,Andreas P Teske,Kelly C Wrighton,S Emil Ruff,Marc Strous,Mikayla A Borton,Isabella Hrabe De Angelis

doi:10.1038/s41396-021-01026-5

Abstract

Hydrothermal sediments contain large numbers of uncultured heterotrophic microbial lineages. Here, we amended Guaymas Basin sediments with proteins, polysaccharides, nucleic acids or lipids under different redox conditions and cultivated heterotrophic thermophiles with the genomic potential for macromolecule degradation. We reconstructed 20 metagenome-assembled genomes (MAGs) of uncultured lineages affiliating with known archaeal and bacterial phyla, including endospore-forming Bacilli and candidate phylum Marinisomatota. One Marinisomatota MAG had 35 different glycoside hydrolases often in multiple copies, seven extracellular CAZymes, six polysaccharide lyases, and multiple sugar transporters. This population has the potential to degrade a broad spectrum of polysaccharides including chitin, cellulose, pectin, alginate, chondroitin, and carrageenan. We also describe thermophiles affiliating with the genera Thermosyntropha, Thermovirga, and Kosmotoga with the capability to make a living on nucleic acids, lipids, or multiple macromolecule classes, respectively. Several populations seemed to lack extracellular enzyme machinery and thus likely scavenged oligo- or monomers (e.g., MAGs affiliating with Archaeoglobus) or metabolic products like hydrogen (e.g., MAGs affiliating with Thermodesulfobacterium or Desulforudaceae). The growth of methanogens or the production of methane was not observed in any condition, indicating that the tested macromolecules are not degraded into substrates for methanogenesis in hydrothermal sediments. We provide new insights into the niches, and genomes of microorganisms that actively degrade abundant necromass macromolecules under oxic, sulfate-reducing, and fermentative thermophilic conditions. These findings improve our understanding of the carbon flow across trophic levels and indicate how primary produced biomass sustains complex and productive ecosystems.

Highlights

Influenced marine sediments are characterized by fluctuating temperatures, and inorganic and organic carbon substrates that can support a diverse range of microbial metabolic activities [1,2,3]
Enriched bacterial and archaeal lineages and their catabolic potential were analyzed by 16S rRNA gene and metagenomic analyses (Fig. 1D), methane and hydrogen production was measured using gas chromatography and growth was estimated using cell counts
We show that Guaymas Basin hydrothermal sediments host a variety of thermophilic heterotrophs with the potential to hydrolyze the tested cellular macromolecules and transport their oligomers

Summary

Introduction

Influenced marine sediments are characterized by fluctuating temperatures, and inorganic and organic carbon substrates that can support a diverse range of microbial metabolic activities [1,2,3]. A substantial proportion of the diversity and community function at hydrothermal systems is attributed to heterotrophic microorganisms [6, 7]. This heterotrophic community comprises many uncultured and understudied lineages which likely meet their carbon and energy demands using biological macromolecules such as proteins [8], nucleic acids [9], lipids [10], and polysaccharides [11]. Identifying the microorganisms and enzymes involved in the degradation of macromolecules in hydrothermal sediments is relevant for our understanding of biogeochemical cycling and ecosystem functioning in deep-sea environments

Methods

Results

Discussion

Conclusion