Engineering topics

Martens-Habbena, Willm

Publications and source records attributed to Martens-Habbena, Willm.

6 records

DOE OSTI2024

Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences

Ammonia-oxidizing microorganisms (AOM) contribute to one of the largest nitrogen fluxes in the global nitrogen budget. Four distinct lineages of AOM: ammonia-oxidizing archaea (AOA), beta- and gamma-proteobacterial ammonia-oxidizing bacteria (β-AOB and γ-AOB) and complete ammonia oxidizers (comammox), are thought to compete for ammonia as their primary nitrogen substrate. In addition, many AOM species can utilize urea as an alternative energy and nitrogen source through hydrolysis to ammonia. How the coordination of ammonia and urea metabolism in AOM influences their ecology remains poorly understood. Here we use stable isotope tracing, kinetics and transcriptomics experiments to show that representatives of the AOM lineages employ distinct regulatory strategies for ammonia or urea utilization, thereby minimizing direct substrate competition. The tested AOA and comammox species preferentially used ammonia over urea, while β-AOB favoured urea utilization, repressed ammonia transport in the presence of urea and showed higher affinity for urea than for ammonia. Characterized γ-AOB co-utilized both substrates. Furthermore, these results reveal contrasting niche adaptation and coexistence patterns among the major AOM lineages.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments

Ammonia-oxidizing archaea (AOA) are among the most ubiquitous and abundant archaea on Earth, widely distributed in marine, terrestrial, and geothermal ecosystems. However, the genomic diversity, biogeography, and evolutionary process of AOA populations in subsurface environments are vastly understudied compared to those in marine and soil systems. Here, we report a novel AOA order Candidatus (Ca.) Nitrosomirales which forms a sister lineage to the thermophilic Ca. Nitrosocaldales. Metagenomic and 16S rRNA gene-read mapping demonstrates the abundant presence of Nitrosomirales AOA in various groundwater environments and their widespread distribution across a range of geothermal, terrestrial, and marine habitats. Terrestrial Nitrosomirales AOA show the genetic capacity of using formate as a source of reductant and using nitrate as an alternative electron acceptor. Nitrosomirales AOA appear to have acquired key metabolic genes and operons from other mesophilic populations via horizontal gene transfer, including genes encoding urease, nitrite reductase, and V-type ATPase. The additional metabolic versatility conferred by acquired functions may have facilitated their radiation into a variety of subsurface, marine, and soil environments. We also provide evidence that each of the four AOA orders spans both marine and terrestrial habitats, which suggests a more complex evolutionary history for major AOA lineages than previously proposed. Together, these findings establish a robust phylogenomic framework of AOA and provide new insights into the ecology and adaptation of this globally abundant functional guild.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Nitrogen and phosphorous acquisition strategies drive coexistence patterns among archaeal lineages in soil

Soil represents the largest reservoir of Archaea on Earth. Present-day archaeal diversity in soils globally is dominated by members of the class Nitrososphaeria. The evolutionary radiation of this class is thought to reflect adaptations to a wide range of temperatures, pH, and other environmental conditions. However, the mechanisms that govern competition and coexistence among Nitrososphaeria lineages in soil remain poorly understood. Here we show that predominant soil Nitrososphaeria lineages compose a patchwork of gene inventory and expression profiles for ammonia, urea, and phosphate utilization. In contrast, carbon fixation, respiration, and ATP synthesis genes are conserved and expressed consistently among predominant phylotypes across 12 major evolutionary lineages commonly found in soil. In situ gene expression profiles closely resemble pure culture reference strains under optimal growth conditions. Together, these results reveal resource-based coexistence patterns among Nitrososphaeria lineages and suggest complementary ecophysiological niches associated with differential nutrient acquisition strategies among globally predominant archaeal lineages in soil.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Fine-scale evaluation of two standard 16S rRNA gene amplicon primer pairs for analysis of total prokaryotes and archaeal nitrifiers in differently managed soils

The advance of high-throughput molecular biology tools allows in-depth profiling of microbial communities in soils, which possess a high diversity of prokaryotic microorganisms. Amplicon-based sequencing of 16S rRNA genes is the most common approach to studying the richness and composition of soil prokaryotes. To reliably detect different taxonomic lineages of microorganisms in a single soil sample, an adequate pipeline including DNA isolation, primer selection, PCR amplification, library preparation, DNA sequencing, and bioinformatic post-processing is required. Besides DNA sequencing quality and depth, the selection of PCR primers and PCR amplification reactions arguably have the largest influence on the results. This study tested the performance and potential bias of two primer pairs, i.e., 515F (Parada)-806R (Apprill) and 515F (Parada)-926R (Quince) in the standard pipelines of 16S rRNA gene Illumina amplicon sequencing protocol developed by the Earth Microbiome Project (EMP), against shotgun metagenome-based 16S rRNA gene reads. The evaluation was conducted using five differently managed soils. We observed a higher richness of soil total prokaryotes by using reverse primer 806R compared to 926R, contradicting to in silico evaluation results. Both primer pairs revealed various degrees of taxon-specific bias compared to metagenome-derived 16S rRNA gene reads. Nonetheless, we found consistent patterns of microbial community variation associated with different land uses, irrespective of primers used. Total microbial communities, as well as ammonia oxidizing archaea (AOA), the predominant ammonia oxidizers in these soils, shifted along with increased soil pH due to agricultural management. In the unmanaged low pH plot abundance of AOA was dominated by the acid-tolerant NS-Gamma clade, whereas limed agricultural plots were dominated by neutral-alkaliphilic NS-Delta/NS-Alpha clades. This study stresses how primer selection influences community composition and highlights the importance of primer selection for comparative and integrative studies, and that conclusions must be drawn with caution if data from different sequencing pipelines are to be compared.

16S rRNA gene amplicon Illumina sequencing↗

DOE OSTI2022

Year-around survey and manipulation experiments reveal differential sensitivities of soil prokaryotic and fungal communities to saltwater intrusion in Florida Everglades wetlands

Global sea-level rise is transforming coastal ecosystems, especially freshwater wetlands, in part due to increased episodic or chronic saltwater exposure, leading to shifts in biogeochemistry, plant- and microbial communities, as well as ecological services. Yet, it is still difficult to predict how soil microbial communities respond to the saltwater exposure because of poorly understood microbial sensitivity within complex wetland soil microbial communities, as well as the high spatial and temporal heterogeneity of wetland soils and saltwater exposure. To address this, we first conducted a two-year survey of microbial community structure and bottom water chemistry in submerged surface soils from 14 wetland sites across the Florida Everglades. We identified ecosystem-specific microbial biomarker taxa primarily associated with variation in salinity. Bacterial, archaeal and fungal community composition differed between freshwater, mangrove, and marine seagrass meadow sites, irrespective of soil type or season. Especially, methanogens, putative denitrifying methanotrophs and sulfate reducers shifted in relative abundance and/or composition between wetland types. Methanogens and putative denitrifying methanotrophs declined in relative abundance from freshwater to marine wetlands, whereas sulfate reducers showed the opposite trend. A four-year experimental simulation of salt-water intrusion in a pristine freshwater site and a previously saltwater-impacted site corroborated the highest sensitivity and relative increase of sulfate reducers, as well as taxon-specific sensitivity of methanogens, in response to continuously pulsing of saltwater treatment. Collectively, these results suggest that besides increased salinity, saltwater-mediated increased sulfate availability leads to displacement of methanogens by sulfate reducers even at low or temporal salt exposure. In conclusion, these changes of microbial composition could affect organic matter degradation pathways in coastal freshwater wetlands exposed to sea-level rise, with potential consequences, such as loss of stored soil organic carbon.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2020

Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea

Ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms in the ocean, exerting primary control on nitrification and nitrogen oxides emission. Although united by a common physiology of chemoautotrophic growth on ammonia, a corresponding high genomic and habitat variability suggests tremendous adaptive capacity. Here, we compared 44 diverse AOA genomes, 37 from species cultivated from samples collected across diverse geographic locations and seven assembled from metagenomic sequences from the mesopelagic to hadopelagic zones of the deep ocean. Comparative analysis identified seven major marine AOA genotypic groups having gene content correlated with their distinctive biogeographies. Phosphorus and ammonia availabilities as well as hydrostatic pressure were identified as selective forces driving marine AOA genotypic and gene content variability in different oceanic regions. Notably, AOA methylphosphonate biosynthetic genes span diverse oceanic provinces, reinforcing their importance for methane production in the ocean. Together, our combined comparative physiological, genomic, and metagenomic analyses provide a comprehensive view of the biogeography of globally abundant AOA and their adaptive radiation into a vast range of marine and terrestrial habitats.

59 BASIC BIOLOGICAL SCIENCES↗