More Like this

1. Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean

   https://doi.org/10.1128/mSystems.00415-20  

   Aylward, Frank O.; Santoro, Alyson E.; Bouskill, Nick (June 2020, mSystems)

   ABSTRACT The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage. 

   more » « less
2. Differentiated Evolutionary Strategies of Genetic Diversification in Atlantic and Pacific Thaumarchaeal Populations

   https://doi.org/10.1128/msystems.01477-21  

   Hwang, Yunha; Girguis, Peter R. (June 2022, mSystems)

   Bowman, Jeff (Ed.)

   ABSTRACT Some marine microbes are seemingly “ubiquitous,” thriving across a wide range of environmental conditions. While the increased depth in metagenomic sequencing has led to a growing body of research on within-population heterogeneity in environmental microbial populations, there have been fewer systematic comparisons and characterizations of population-level genetic diversity over broader expanses of time and space. Here, we investigated the factors that govern the diversification of ubiquitous microbial taxa found within and between ocean basins. Specifically, we use mapped metagenomic paired reads to examine the genetic diversity of ammonia-oxidizing archaeal (“ Candidatus Nitrosopelagicus brevis”) populations in the Pacific (Hawaii Ocean Time-series [HOT]) and Atlantic (Bermuda Atlantic Time Series [BATS]) Oceans sampled over 2 years. We observed higher nucleotide diversity in “ Ca. N. brevis” at HOT, driven by a higher rate of homologous recombination. In contrast, “ Ca. N. brevis” at BATS featured a more open pangenome with a larger set of genes that were specific to BATS, suggesting a history of dynamic gene gain and loss events. Furthermore, we identified highly differentiated genes that were regulatory in function, some of which exhibited evidence of recent selective sweeps. These findings indicate that different modes of genetic diversification likely incur specific adaptive advantages depending on the selective pressures that they are under. Within-population diversity generated by the environment-specific strategies of genetic diversification is likely key to the ecological success of “ Ca. N. brevis.” IMPORTANCE Ammonia-oxidizing archaea (AOA) are one of the most abundant chemolithoautotrophic microbes in the marine water column and are major contributors to global carbon and nitrogen cycling. Despite their ecological importance and geographical pervasiveness, there have been limited systematic comparisons and characterizations of their population-level genetic diversity over time and space. Here, we use metagenomic time series from two ocean observatories to address the fundamental questions of how abiotic and biotic factors shape the population-level genetic diversity and how natural microbial populations adapt across diverse habitats. We show that the marine AOA “ Candidatus Nitrosopelagicus brevis” in different ocean basins exhibits distinct modes of genetic diversification in response to their selective regimes shaped by nutrient availability and patterns of environmental fluctuations. Our findings specific to “ Ca. N. brevis” have broader implications, particularly in understanding the population-level responses to the changing climate and predicting its impact on biogeochemical cycles. 

   more » « less
3. Substrate Effect on the Contribution of Ammonium and Urea to Marine Nitrification and Nitrous Oxide Production

   https://doi.org/10.1111/1462-2920.70187  

   Tang, Weiyi; Hexter, Catherine; Dai, Rongbo; Fortin, Samantha G; Tracey, John C; Intrator, Naomi; Kunes, Moriah A; Wan, Xianhui S; Jayakumar, Amal; Shi, Dalin; et al (October 2025, Environmental Microbiology)

   ABSTRACT Nitrification (microbial oxidation of ammonia to nitrite and nitrate) controls nitrogen speciation and is the main source of nitrous oxide (N₂O) in the ocean. It was recently shown that the most abundant marine ammonia oxidizers, the ammonia‐oxidising archaea (AOA), are also capable of oxidising urea, providing a previously ignored source of nitrite. Here, we show that the relative magnitude of urea and ammonia oxidation rates, and the relative rates of N₂O production from the two substrates, is correlated with the ratio of the substrate concentrations. By examining all reported measurements of urea and ammonium concentrations and the paired urea and ammonia oxidation rates, we show that this relationship likely holds across the global ocean. Examination of newly acquired and previously published metagenomic data shows that the fraction of AOA with the genetic capability for urea oxidation increases with the urea:ammonium ratio, rather than depending on the urea or ammonium concentration alone. These results corroborate the correlation between substrate ratios and oxidation rate ratios, and extend it to N₂O production. This may help explain the distribution of nitrification rates and N₂O production in the ocean. 

   more » « less
4. Diversity and Evolution of Pigment Types in Marine Synechococcus Cyanobacteria

   https://doi.org/10.1093/gbe/evac035  

   Grébert, Théophile; Garczarek, Laurence; Daubin, Vincent; Humily, Florian; Marie, Dominique; Ratin, Morgane; Devailly, Alban; Farrant, Gregory K; Mary, Isabelle; Mella-Flores, Daniella; et al (April 2022, Genome Biology and Evolution)

   Angert, Esther (Ed.)

   Abstract Synechococcus cyanobacteria are ubiquitous and abundant in the marine environment and contribute to an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core, from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus cells to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examine the variability of gene content and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements for DNA integration and site-specific recombination, suggesting that their genomic variability relies in part on a “tycheposon”-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the core genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of incomplete lineage sorting in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events. 

   more » « less
5. Ocean warming enhances iron use efficiencies of marine ammonia-oxidizing archaea

   https://doi.org/10.1073/pnas.2531032123  

   Qin, Wei; Tagliabue, Alessandro; Hou, Lei; Xu, Min; Bian, Xiaopeng; Moran, Dawn M; Zhao, Duo; Li, Qian; McIlvin, Matthew R; Zheng, Yue; et al (March 2026, Proceedings of the National Academy of Sciences)

   Ammonia-oxidizing archaea (AOA) are among the most abundant microorganisms in the ocean, playing a fundamental role in the marine nitrogen cycle. Although temperature and trace metal availability each individually influence the growth and activity of marine AOA, there is only a very limited understanding of the interactive effects of these two major factors on AOA in the rapidly changing ocean. Here, we show that the iron requirements of the model marine AOA speciesNitrosopumilus maritimusSCM1 are highly sensitive to temperature changes. A 5 °C increase in growth temperature reduced SCM1 iron requirements by >80%, and was associated with a substantial increase in iron use efficiencies (IUE, mol C fixed/h/mol cellular Fe) under iron-limited and warming conditions. A thermally enhanced IUE enables SCM1 to more efficiently utilize scarce available iron supplies to support its growth. Whole-cell proteomic analysis revealed that iron limitation decreased expression of a ferredoxin and increased expression of a copper-dependent plastocyanin that became more pronounced with warming, suggesting coordinated electron transport response regulation under combined iron and temperature stress. The global impacts of these temperature-dependent changes to AOA iron demands were assessed using sensitivity experiments with a state-of-the-art biogeochemical model. Simulations showed that impacts on nitrification were concentrated at higher latitudes, but the alterations to ammonia concentrations were redistributed toward lower latitudes by mode and intermediate water transport. These findings reveal a previously unrecognized mechanism by which ocean warming may alleviate iron limitation of AOA, enhance their ecological competitiveness, and reshape ocean nitrogen cycling throughout marine ecosystems. 

   more » « less