Abstract Microorganisms have evolved diverse strategies to acquire the vital element nitrogen (N) from the environment. Ecological and physiological controls on the distribution of these strategies among microbes remain unclear. In this study, we examine the distribution of 10 major N acquisition strategies in taxonomically and metabolically diverse microbial genomes, including those from the Genomic Catalogue of Earth's Microbiomes dataset. We utilize a marker gene‐based approach to assess relationships between N acquisition strategy prevalence and microbial life history strategies. Our results underscore energetic costs of assimilation as a broad control on strategy distribution. The most prevalent strategies are the uptake of ammonium and simple amino acids, which have relatively low energetic costs, while energy‐intensive biological nitrogen fixation is the least common. Deviations from the energy‐based framework include the higher‐than‐expected prevalence of the assimilatory pathway for chitin, a large organic polymer. Energy availability is also important, with aerobic chemoorganotrophs and oxygenic phototrophs notably possessing ~2‐fold higher numbers of total strategies compared to anaerobic microbes. Environmental controls are evidenced by the enrichment of inorganic N assimilation strategies among free‐living taxa compared to host‐associated taxa. Physiological constraints such as pathway incompatibility add complexity to N acquisition strategy distributions. Finally, we discuss the necessity for microbially‐relevant spatiotemporal environmental metadata for improving mechanistic and prediction‐oriented analyses of genomic data.
Abstract Nitrification plays a key role in marine ecosystems where Thaumarchaeota are thought to be responsible for most of the ammonia oxidation in the water column. Over a 2‐yr, near‐monthly time series at two sites in Monterey Bay we observed repeatable seasonal and depth‐based patterns of Thaumarchaeota ecotype abundance that highlighted a clear delineation between populations in shallow euphotic (< 50 m) vs. deeper mesopelagic (60–500 m) depths. Euphotic depths show greater seasonality and influence from light, while mesopelagic waters have trends based on water mass and other covarying features with depth. Three major ecotypes were recovered: a Nitrosopumilus ‐like (NP) group, a Nitrosopelagicus ‐like ecotype containing “shallow” water column A (WCA) members, and an ecotype affiliated with the “deep” water column B (WCB) Thaumarchaeota . These ecotypes show a strong depth distribution, with WCB dominant at ≥ 200 m depth and WCA most abundant in surface (5–100 m) waters. The NP ecotype was found throughout the water column with the highest abundance in summer, and was the only ecotype showing a correlation with measured nitrification rates. We also found three abundant taxa related to Nitrospina —the major nitrite‐oxidizing bacteria in the ocean; these showed clear connections to each of the three Thaumarchaeota ecotypes, suggesting a specific relationship between both steps of nitrification. Our results support the importance of ecotype‐based analysis of Thaumarchaeota and show that their abundance and distribution are controlled based on their water column position, with a distinct shift at 50 m between euphotic and mesopelagic depths.
<p>Biological nitrogen fixation (BNF) is a critical process for the N budget and productivity of marine ecosystems. Nitrogen-fixing organisms typically turn off BNF when less metabolically costly N sources, like ammonium (NH<sub>4</sub><sup>+</sup>), are available. Yet, several studies have reported BNF in benthic marine sediments despite high porewater NH<sub>4</sub><sup>+</sup> concentrations (10-1,500 &#181;M). These activities were generally linked to anaerobic sulfate-reducing bacteria (SRB) and fermenting firmicutes.</p><p>To better understand the regulation and importance of benthic marine BNF, we evaluate the sensitivity of BNF to NH<sub>4</sub><sup>+</sup> in benthic diazotrophs using incubations of increasing complexity. We conduct our experiment with cultures of model anaerobic diazotrophs (sulfate-reducer <em>Desulfovibrio vulgaris</em> var. Hildenborough, fermenter <em>Clostridium pasteurianum </em>strain W5), sulfate-reducing sediment enrichment cultures, and slurry incubations of sediments from three Northeastern salt marshes (USA).</p><p>All our samples demonstrate high sensitivity to external NH<sub>4</sub><sup>+</sup>. BNF is inhibited by NH<sub>4</sub><sup>+ </sup>beyond an apparent<strong> </strong>threshold [NH<sub>4</sub><sup>+</sup>] of 2 &#181;M in liquid cultures and 9 &#181;M in sediment slurries. Consistent with other studies, we find SRB-like nitrogenase (<em>nifH</em>) gene and transcripts are prevalent in sediments. We compare our inhibition threshold value with a survey of porewater NH<sub>4</sub><sup>+</sup> data from diverse sediments, suggesting the confinement of benthic BNF to surficial sediments.</p><p>Variations in the timing to onset BNF inhibition, NH<sub>4</sub><sup>+</sup> uptake rate, and sediment composition and biophysics could affect measurements of the apparent<strong> </strong>sensitivity of benthic BNF to NH<sub>4</sub><sup>+</sup>. We propose a simple model based on NH<sub>4</sub><sup>+</sup> transporter affinity as a fundamental mechanistic constraint on NH<sub>4</sub><sup>+</sup> control of BNF to improve biogeochemical models of N cycling.</p>
Understanding microbial niche differentiation along ecological and geochemical gradients is critical for assessing the mechanisms of ecosystem response to hydrologic variation and other aspects of global change. The lineage-specific biogeochemical roles of the widespread phylum Acidobacteria in hydrologically sensitive ecosystems, such as peatlands, are poorly understood. Here, we demonstrate that Acidobacteria sublineages in Sphagnum peat respond differentially to redox fluctuations due to variable oxygen (O2) availability, a typical feature of hydrologic variation. Our genome-centric approach disentangles the mechanisms of niche differentiation between the Acidobacteria genera Holophaga and Terracidiphilus in response to the transient O2 exposure of peat in laboratory incubations. Interlineage functional diversification explains the enrichment of the otherwise rare Holophaga in anoxic peat after transient O2 exposure in comparison to Terracidiphilus dominance in continuously anoxic peat. The observed niche differentiation of the two lineages is linked to differences in their carbon degradation potential. Holophaga appear to be primarily reliant on carbohydrate oligomers and amino acids, produced during the prior period of O2 exposure via the O2-stimulated breakdown of peat carbon, rich in complex aromatics and carbohydrate polymers. In contrast, Terracidiphilus genomes are enriched in diverse respiratory hydrogenases and carbohydrate active enzymes, enabling the degradation of complex plant polysaccharides into monomers and oligomers for fermentation. We also present the first evidence for the potential contribution of Acidobacteria in peat nitrogen fixation. In addition to canonical molybdenum-based diazotrophy, the Acidobacteria genomes harbor vanadium and iron-only alternative nitrogenases. Together, the results better inform the different functional roles of Acidobacteria in peat biogeochemistry under global change. IMPORTANCE Acidobacteria are among the most widespread and abundant members of the soil bacterial community, yet their ecophysiology remains largely underexplored. In acidic peat systems, Acidobacteria are thought to perform key biogeochemical functions, yet the mechanistic links between the phylogenetic and metabolic diversity within this phylum and peat carbon transformations remain unclear. Here, we employ genomic comparisons of Acidobacteria subgroups enriched in laboratory incubations of peat under variable O2 availability to disentangle the lineage-specific functional roles of these microorganisms in peat carbon transformations. Our genome-centric approach reveals that the diversification of Acidobacteria subpopulations across transient O2 exposure is linked to differences in their carbon substrate preferences. We also identify a previously unknown functional potential for biological nitrogen fixation in these organisms. This has important implications for carbon, nitrogen, and trace metal cycling in peat systems.
ABSTRACT Microorganisms have evolved diverse strategies to acquire the vital element nitrogen (N) from the environment. Ecological and physiological controls on the distribution of these strategies among microbes remain unclear. Here we examine the distribution of 10 major N-acquisition strategies in taxonomically and metabolically diverse microbial genomes, including those from the Genomic Catalog of Earth’s Microbiomes dataset. We utilize a marker gene-based approach to assess relationships between N acquisition strategy prevalence and microbial life history strategies. Our results underscore energetic costs of assimilation as a broad control on strategy distribution. The most prevalent strategies are the uptake of ammonium and simple amino acids, while biological nitrogen fixation is the least common. Deviations from this energy-based framework include the higher-than-expected prevalence of the assimilatory pathway for chitin, a large organic polymer. Notably, oxygen-respiring chemoorganotrophic and phototrophic microbes possess ∼2-fold higher numbers of total strategies compared to anaerobic microbes. Environmental controls on N acquisition are evidenced by the enrichment of inorganic N assimilation strategies among free-living taxa compared to host-associated taxa. Physiological constrains such as pathway incompatibility add further complexity to N-acquisition strategy distributions. Finally, we discuss the necessity for microbially-relevant environmental metadata for improving mechanistic and prediction-oriented analyses of genomic data.
Coastal upwelling regions are hotspots of biological productivity, supporting diverse communities of microbial life and metabolisms. Monterey Bay (MB), a coastal ocean embayment in central California, experiences seasonal upwelling of cold, nutrient-rich waters that sustain episodes of high phytoplankton production in surface waters. While productivity in surface waters is intimately linked to metabolisms of diverse communities of Archaea and Bacteria, a comprehensive understanding of the microbial community in MB is missing thus far, particularly in relation to the distinct hydrographic seasons characteristic of the MB system. Here we present the results of a two-year microbial time-series survey in MB, investigating community composition and structure across spatiotemporal gradients. In deciphering these patterns, we used unique sequence variants (SVs) of the 16S rRNA gene (V4-V5 region), complemented with metagenomes and metatranscriptomes representing multiple depth profiles. We found clear depth-differentiation and recurring seasonal abundance patterns within planktonic communities, particularly when analyzed at finer taxonomic levels. Compositional changes were more pronounced in the upper 0 - 40 m of the water column, whereas deeper depths were characterized by temporally stable populations. In accordance with the dynamic nutrient profiles, the system appears to change from a Bacteroidetes- and Rhodobacterales-dominated upwelling period to an oceanic season dominated by oligotrophic groups such as SAR11 and picocyanobacteria. The cascade of environmental changes brought about by upwelling and relaxation events thus impacts microbial community structure in the bay, with important implications for the temporal variability of nutrient and energy fluxes within the MB ecosystem. Our observations emphasize the need for continued monitoring of planktonic microbial communities in order to predict and manage the behavior of this sensitive marine sanctuary ecosystem, over projected intensification of upwelling in the region.
Abstract New bioavailable nitrogen (N) from biological nitrogen fixation (BNF) is critical for the N budget and productivity of marine ecosystems. Nitrogen‐fixing organisms typically inactivate BNF when less metabolically costly N sources, like ammonium (NH 4 + ), are available. Yet, several studies have observed BNF in benthic marine sediments linked to anaerobic sulfate‐reducing bacteria and fermenting firmicutes despite high porewater NH 4 + concentrations (10–1,500 μM). To better understand the regulating controls and importance of benthic marine BNF, we evaluate BNF sensitivity to NH 4 + in benthic diazotrophs using incubations of increasing biogeochemical complexity. BNF by cultures of model anaerobic diazotrophs (sulfate‐reducer Desulfovibrio vulgaris var. Hildenborough, fermenter Clostridium pasteurianum strain W5), sulfate‐reducing sediment enrichment cultures, and sediments from three Northeastern salt marshes (USA) is highly sensitive to external NH 4 + . BNF is inhibited by NH 4 + beyond an apparent threshold [NH 4 + ] of 2 μM in liquid cultures, most closely reflecting the true cellular sensitivity of BNF to NH 4 + . Sediment slurries exhibited an apparent threshold [NH 4 + ] of 9 μM. Consistent with other studies, we find SRB‐like nitrogenase ( nifH ) gene and transcripts are prevalent in sediments. Our survey of porewater NH 4 + data from diverse sediments suggests the broad applicability of inhibition thresholds measured here and confinement of benthic BNF to surficial sediments. Variations in BNF inhibition timing, NH 4 + uptake rate, sediment composition, and biophysics could affect measurements of the apparent sensitivity of benthic BNF to NH 4 + . We propose NH 4 + transporter affinity as a fundamental mechanistic constraint on NH 4 + control of cellular BNF to improve biogeochemical models of N cycling.
