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Despite a rising interest in the diversity and ecology of fungi in marine environments, there are few published genomes of fungi isolated from the ocean. The basidiomycetous yeast (unicellular fungus) genusRhodotorulaare prevalent and abundant in the open ocean, and they have been isolated from a wide range of other environments. Many of these environments are nutrient poor, such as the Antarctica and the Atacama deserts, raising the question as to howRhodotorulayeasts may have adapted their metabolic strategies to optimize survival under low nutrient conditions. In order to understand their adaptive strategies in the ocean, the genome ofR. sphaerocarpaETNP2018 was compared to that of fourteen representativeRhodotorulayeasts, isolated from a variety of environments.

Rhodotorula sphaerocarpaETNP2018, a strain isolated from the oligotrophic part of the eastern tropical North Pacific (ETNP) oxygen minimum zone (OMZ), hosts the smallest of the fifteen genomes and yet the number of protein-coding genes it possesses is on par with the other strains. Its genome exhibits a distinct reduction in genes dedicated to Major Facilitator Superfamily transporters as well as biosynthetic enzymes. However, its core metabolic pathways are fully conserved. Our research indicates that the selective pressures of the ETNP OMZ favor a streamlined genome with reduced overall biosynthetic potential balanced by a stable set of core metabolisms and an expansion of mechanisms for nutrient acquisition.

In summary, this study offers insights into the adaptation of fungi to the oligotrophic ocean and provides valuable information for understanding the ecological roles of fungi in the ocean.

 

Abstract. The Santa Barbara Basin naturally experiences transient deoxygenation due to its unique geological setting in the southern California Borderland and seasonal changes in ocean currents. Long-term measurements of the basin showed that anoxic events and subsequent nitrate exhaustion in the bottom waters have been occurring more frequently and lasting longer over the past decade. One characteristic of the Santa Barbara Basin is the seasonal development of extensive mats of benthic nitrate-reducing sulfur-oxidizing bacteria, which are found at the sediment–water interface when the basin's bottom waters reach anoxia but still provide some nitrate. To assess the mat's impact on the benthic and pelagic redox environment, we collected biogeochemical sediment and benthic flux data in November 2019, after anoxia developed in the deepest waters of the basin and dissolved nitrate was depleted (down to 9.9 µM). We found that the development of mats was associated with a shift from denitrification to dissimilatory nitrate reduction to ammonium. The zone of sulfate reduction appeared near the sediment–water interface in sediment hosting these ephemeral white mats. We found that an exhaustion of iron oxides in the surface sediment was an additional prerequisite for mat proliferation. Our research further suggests that cycles of deoxygenation and reoxygenation of the benthic environment result in extremely high benthic fluxes of dissolved iron from the basin's sediment. This work expands our understanding of nitrate-reducing sulfur-oxidizing mats and their role in sustaining and potentially expanding marine anoxia.

 

Abstract. As a key biogeochemical pathway in the marine nitrogen cycle, nitrification (ammonia oxidation and nitrite oxidation) converts the most reduced form of nitrogen – ammonium–ammonia (NH4+–NH3) – into the oxidized species nitrite (NO2-) and nitrate (NO3-). In the ocean, these processes are mainly performed by ammonia-oxidizing archaea (AOA) and bacteria (AOB) and nitrite-oxidizing bacteria (NOB). By transforming nitrogen speciation and providing substrates for nitrogen removal, nitrification affects microbial community structure; marine productivity (including chemoautotrophic carbon fixation); and the production of a powerful greenhouse gas, nitrous oxide (N2O). Nitrification is hypothesized to be regulated by temperature, oxygen, light, substrate concentration, substrate flux, pH and other environmental factors. Although the number of field observations from various oceanic regions has increased considerably over the last few decades, a global synthesis is lacking, and understanding how environmental factors control nitrification remains elusive. Therefore, we have compiled a database of nitrification rates and nitrifier abundance in the global ocean from published literature and unpublished datasets. This database includes 2393 and 1006 measurements of ammonia oxidation and nitrite oxidation rates and 2242 and 631 quantifications of ammonia oxidizers and nitrite oxidizers, respectively. This community effort confirms and enhances our understanding of the spatial distribution of nitrification and nitrifiers and their corresponding drivers such as the important role of substrate concentration in controlling nitrification rates and nitrifier abundance. Some conundrums are also revealed, including the inconsistent observations of light limitation and high rates of nitrite oxidation reported from anoxic waters. This database can be used to constrain the distribution of marine nitrification, to evaluate and improve biogeochemical models of nitrification, and to quantify the impact of nitrification on ecosystem functions like marine productivity and N2O production. This database additionally sets a baseline for comparison with future observations and guides future exploration (e.g., measurements in the poorly sampled regions such as the Indian Ocean and method comparison and/or standardization). The database is publicly available at the Zenodo repository: https://doi.org/10.5281/zenodo.8355912 (Tang et al., 2023).

 

Fungi in terrestrial environments are known to play a key role in carbon and nitrogen biogeochemistry and exhibit high diversity. In contrast, the diversity and function of fungi in the ocean has remained underexplored and largely neglected. In the eastern tropical North Pacific oxygen minimum zone, we examined the fungal diversity by sequencing the internal transcribed spacer region 2 (ITS2) and mining a metagenome dataset collected from the same region. Additionally, we coupled 15N-tracer experiments with a selective inhibition method to determine the potential contribution of marine fungi to nitrous oxide (N2O) production. Fungal communities evaluated by ITS2 sequencing were dominated by the phyla Basidiomycota and Ascomycota at most depths. However, the metagenome dataset showed that about one third of the fungal community belong to early-diverging phyla. Fungal N2O production rates peaked at the oxic–anoxic interface of the water column, and when integrated from the oxycline to the top of the anoxic depths, fungi accounted for 18–22% of total N2O production. Our findings highlight the limitation of ITS-based methods typically used to investigate terrestrial fungal diversity and indicate that fungi may play an active role in marine nitrogen cycling. 

Changes in the sequence of an organism’s genome, i.e., mutations, are the raw material of evolution. The frequency and location of mutations can be constrained by specific molecular mechanisms, such as diversity-generating retroelements (DGRs). DGRs have been characterized from cultivated bacteria and bacteriophages, and perform error-prone reverse transcription leading to mutations being introduced in specific target genes. DGR loci were also identified in several metagenomes, but the ecological roles and evolutionary drivers of these DGRs remain poorly understood. Here, we analyze a dataset of >30,000 DGRs from public metagenomes, establish six major lineages of DGRs including three primarily encoded by phages and seemingly used to diversify host attachment proteins, and demonstrate that DGRs are broadly active and responsible for >10% of all amino acid changes in some organisms. Overall, these results highlight the constraints under which DGRs evolve, and elucidate several distinct roles these elements play in natural communities.