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

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.

Extremely thermophilic endospores germinate and metabolise organic carbon in sediments heated to above 80°C

“…Purines from dead cells offer another source of organic carbon and nitrogen as Thermanaeromonas had the potential to degrade xanthine, a nitrogen-rich organic compound from nucleic acids that is widespread in aquatic environments (Cunliffe, 2016). Thermosediminibacteraceae, Symbiobacteriales and Thermoanaeromonas genomes all contained an extracellular nuclease for degradation of DNA polymers and all MAGs contained nucleoside and nucleobase transporters that may be used for salvage or as a carbon and energy source (Pérez Castro et al, 2021).…”

“…Thermosediminibacteraceae, Symbiobacteriales and Thermoanaeromonas genomes all contained an extracellular nuclease for degradation of DNA polymers and all MAGs contained nucleoside and nucleobase transporters that may be used for salvage or as a carbon and energy source (Pérez Castro et al, 2021).…”

Microbial Community Response to Polysaccharide Amendment in Anoxic Hydrothermal Sediments of the Guaymas Basin

“…Besides possible biases introduced during cell extract preparation, extracellular DNA, only represented in the DNA extract may contribute to discrepancies in community composition (Couradeau et al, 2019). Deep-sea sediments are known to contain extracellular DNA, which is also considered an important macromolecular carbon source for the heterotrophic microbial community including in Guaymas Basin sediments (Jørgensen and Jacobsen, 1996;Dell'Anno and Danovaro, 2005;Corinaldesi et al, 2007;Perez Castro et al, 2021), but the effect of extracellular DNA on microbial diversity surveys is disputed and not well established (Lever et al, 2015;Carini et al, 2016;Ramírez et al, 2018;Torti et al, 2018).…”

“…Notably, Thermotogae were detected with the highest relative sequence abundance in the active fraction of most mesocosms after 2 days (Figure 2) but the abundant Thermotogae-affiliated ASV (ASV_8d59c) did not show a strong substrate specific response. However, Thermotogae are widespread in marine hydrothermal sediments and some members have recently been implicated in polysaccharide degradation in Guaymas Basin sediments (Perez Castro et al, 2021). In contrast, ASVs affiliated with Thiomicrospiraceae (1), Thiovulaceae (1), Sulfurovaceae (1) and Desulfobulbaceae (1), while abundant in the inoculum, decreased in proportion in the active fraction, suggesting that these organisms initially did not benefit from selected incubation conditions.…”

“…Guaymas Basin sediments contain a variety of organic macromolecules (lipids, proteins, DNA and polysaccharides) (De la Lanza-Espino and Soto, 1999;Teske et al, 2002;Zheng et al, 2021) and harbor a diverse heterotrophic community with the genetic potential to degrade a wide range of these compounds (Dombrowski et al, 2018;Baker et al, 2021;Perez Castro et al, 2021). Polysaccharides are abundant in the ocean and are commonly introduced into sediments from surface waters or terrestrial runoffs or are produced from decaying biomass.…”