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Growing evidence suggests that interactions among heterotrophic microorganisms influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microorganisms inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific polymerase chain reaction (PCR) assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound whereas both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that coincubation of these isolates enhanced organic matter turnover, sometimes by nearly 2-fold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that coincubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition whereas high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.

 

The Guaymas Basin in the Gulf of California is characterized by active seafloor spreading, the rapid deposition of organic-rich sediments, steep geothermal gradients, and abundant methane of mixed thermogenic and microbial origin. Subsurface sediment samples from eight drilling sites with distinct geochemical and thermal profiles were selected for DNA extraction and PCR amplification to explore the diversity of methane-cycling archaea in the Guaymas Basin subsurface. We performed PCR amplifications with general (mcrIRD), and ANME-1 specific primers that target the alpha (α) subunit of methyl coenzyme M reductase (mcrA). Diverse ANME-1 lineages associated with anaerobic methane oxidation were detected in seven out of the eight drilling sites, preferentially around the methane-sulfate interface, and in several cases, showed preferences for specific sampling sites. Phylogenetically, most ANME-1 sequences from the Guaymas Basin subsurface were related to marine mud volcanoes, seep sites, and the shallow marine subsurface. The most frequently recovered methanogenic phylotypes were closely affiliated with the hyperthermophilic Methanocaldococcaceae, and found at the hydrothermally influenced Ringvent site. The coolest drilling site, in the northern axial trough of Guaymas Basin, yielded the greatest diversity in methanogen lineages. Our survey indicates the potential for extensive microbial methane cycling within subsurface sediments of Guaymas Basin.

 

Previous studies of microbial communities in subseafloor sediments reported that microbial abundance and diversity decrease with sediment depth and age, and microbes dominating at depth tend to be a subset of the local seafloor community. However, the existence of geographically widespread, subsurface-adapted specialists is also possible. Here, we use metagenomic and metatranscriptomic analyses of the hydrothermally heated, sediment layers of Guaymas Basin (Gulf of California, Mexico) to examine the distribution and activity patterns of bacteria and archaea along thermal, geochemical and cell count gradients. We find that the composition and distribution of metagenome-assembled genomes (MAGs), dominated by numerous lineages of Chloroflexota and Thermoproteota, correlate with biogeochemical parameters as long as temperatures remain moderate, but downcore increasing temperatures beyond ca. 45 ºC override other factors. Consistently, MAG size and diversity decrease with increasing temperature, indicating a downcore winnowing of the subsurface biosphere. By contrast, specific archaeal MAGs within the Thermoproteota and Hadarchaeota increase in relative abundance and in recruitment of transcriptome reads towards deeper, hotter sediments, marking the transition towards a specialized deep, hot biosphere.

 

Analyses of gene expression of subsurface bacteria and archaea provide insights into their physiological adaptations to in situ subsurface conditions. We examined patterns of expressed genes in hydrothermally heated subseafloor sediments with distinct geochemical and thermal regimes in Guaymas Basin, Gulf of California, Mexico. RNA recovery and cell counts declined with sediment depth, however, we obtained metatranscriptomes from eight sites at depths spanning between 0.8 and 101.9 m below seafloor. We describe the metabolic potential of sediment microorganisms, and discuss expressed genes involved in tRNA, mRNA, and rRNA modifications that enable physiological flexibility of bacteria and archaea in the hydrothermal subsurface. Microbial taxa in hydrothermally influenced settings like Guaymas Basin may particularly depend on these catalytic RNA functions since they modulate the activity of cells under elevated temperatures and steep geochemical gradients. Expressed genes for DNA repair, protein maintenance and circadian rhythm were also identified. The concerted interaction of many of these genes may be crucial for microorganisms to survive and to thrive in the Guaymas Basin subsurface biosphere.

 

Deep marine sediments (>1mbsf) harbor ~26% of microbial biomass and are the largest reservoir of methane on Earth. Yet, the deep subsurface biosphere and controls on its contribution to methane production remain underexplored. Here, we use a multidisciplinary approach to examine methanogenesis in sediments (down to 295 mbsf) from sites with varying degrees of thermal alteration (none, past, current) at Guaymas Basin (Gulf of California) for the first time. Traditional (13C/12C and D/H) and multiply substituted (13CH3D and 12CH2D2) methane isotope measurements reveal significant proportions of microbial methane at all sites, with the largest signal at the site with past alteration. With depth, relative microbial methane decreases at differing rates between sites. Gibbs energy calculations confirm methanogenesis is exergonic in Guaymas sediments, with methylotrophic pathways consistently yielding more energy than the canonical hydrogenotrophic and acetoclastic pathways. Yet, metagenomic sequencing and cultivation attempts indicate that methanogens are present in low abundance. We find only one methyl-coenzyme M (mcrA) sequence within the entire sequencing dataset. Also, we identify a wide diversity of methyltransferases (mtaB, mttB), but only a few sequences phylogenetically cluster with methylotrophic methanogens. Our results suggest that the microbial methane in the Guaymas subsurface was produced over geologic time by relatively small methanogen populations, which have been variably influenced by thermal sediment alteration. Higher resolution metagenomic sampling may clarify the modern methanogen community. This study highlights the importance of using a multidisciplinary approach to capture microbial influences in dynamic, deep subsurface settings like Guaymas Basin.

 

In Guaymas Basin, organic-rich hydrothermal sediments produce complex hydrocarbon mixtures including saturated, aromatic and alkylated aromatic compounds. We examined sediments from push cores from Guyamas sites with distinct temperature and geochemistry profiles to gain a better understanding on abiotic and biological hydrocarbon alteration. Here we provide evidence for biodegradation of hopanoids, producing saturated hydrocarbons like drimane and homodrimane as intermediate products. These sesquiterpene by-products are present throughout cooler sediments, but their relative abundance is drastically reduced within hotter hydrothermal sediments, likely due to hydrothermal mobilization. Within the sterane pool we detect a trend toward aromatization of steroidal compounds within hotter sediments. The changes in hopane and sterane biomarker composition at different sites reflect temperature-related differences in geochemical and microbial hydrocarbon alterations. In contrast to traditionally observed microbial biodegradation patterns that may extend over hundreds of meters in subsurface oil reservoirs, Guaymas Basin shows highly compressed changes in surficial sediments.

 

Life at hydrothermal vent sites is based on chemosynthetic primary producers that supply heterotrophic microorganisms with substrates and generate biomass for higher trophic levels. Often, chemoautotrophs associate with the hydrothermal vent megafauna. To investigate attached bacterial and archaeal communities on deep-sea squat lobsters, we collected ten specimens from a hydrothermal vent in the Guaymas Basin (Gulf of California). All animals were identified asMunidopsis alviscavia morphological and molecular classification, and intraspecific divergence was determined. Amplicon sequencing of microbial DNA and cDNA revealed significant differences between microbial communities on the carapaces ofM. alviscaand those in ambient sea water. Major epibiotic bacterial taxa were chemoautotrophicGammaproteobacteria, such asThiotrichaceaeandMethylococcaceae, while archaea were almost exclusively represented by sequences affiliated withCa. Nitrosopumilus. In sea water samples, Marine Group II and III archaea and organoheterotrophicAlphaproteobacteria,FlavobacteriiaandPlanctomycetaciawere more dominant. Based on the identified taxa, we assume that main metabolic processes, carried out byM. alviscaepibiota, include ammonia, methane and sulphide oxidation. Considering thatM. alviscacould benefit from sulphide detoxification by its epibiota, and that attached microbes are supplied with a stable habitat in proximity to substrate-rich hydrothermal fluids, a mutualistic host-microbe relationship appears likely.

 

ABSTRACT Relatively little is known about the diversity of fungi in deep-sea, hydrothermal sediments. Less thoroughly explored environments are likely untapped reservoirs of unique biodiversity with the potential to augment our current arsenal of microbial compounds with biomedical and/or industrial applications. In this study, we applied traditional culture-based methods to examine a subset of the morphological and phylogenetic diversity of filamentous fungi and yeasts present in 11 hydrothermally influenced sediment samples collected from eight sites on the seafloor of Guaymas Basin, Mexico. A total of 12 unique isolates affiliating with Ascomycota and Basidiomycota were obtained and taxonomically identified on the basis of morphological features and analyses of marker genes including actin, β-tubulin, small subunit ribosomal DNA (18S rRNA), internal transcribed spacer (ITS) and large subunit ribosomal DNA (26S rRNA) D1/D2 domain sequences (depending on taxon). A total of 11 isolates possess congeners previously detected in, or recovered from, deep-sea environments. A total of seven isolates exhibited antibacterial activity against human bacterial pathogens Staphylococcus aureus ATCC-35556 and/or Escherichia coli ATCC-25922. This first investigation suggests that hydrothermal environments may serve as promising reservoirs of much greater fungal diversity, some of which may produce biomedically useful metabolites.