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Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography

Abstract Wetlands store 20–30% of the world’s soil carbon, and identifying the microbial controls on these carbon reserves is essential to predicting feedbacks to climate change. Although viral infections likely play important roles in wetland ecosystem dynamics, we lack a basic understanding of wetland viral ecology. Here 63 viral size-fraction metagenomes (viromes) and paired total metagenomes were generated from three time points in 2021 at seven fresh- and saltwater wetlands in the California Bodega Marine Reserve. We recovered 12,826 viral population genomic sequences (vOTUs), only 4.4% of which were detected at the same field site two years prior, indicating a small degree of population stability or recurrence. Viral communities differed most significantly among the seven wetland sites and were also structured by habitat (plant community composition and salinity). Read mapping to a new version of our reference database, PIGEONv2.0 (515,763 vOTUs), revealed 196 vOTUs present over large geographic distances, often reflecting shared habitat characteristics. Wetland vOTU microdiversity was significantly lower locally than globally and lower within than between time points, indicating greater divergence with increasing spatiotemporal distance. Viruses tended to have broad predicted host ranges via CRISPR spacer linkages to metagenome-assembled genomes, and increased SNP frequencies in CRISPR-targeted major tail protein genes suggest potential viral eco-evolutionary dynamics in response to both immune targeting and changes in host cell receptors involved in viral attachment. Together, these results highlight the importance of dispersal, environmental selection, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography.

Environmental Sciences & Ecology↗

Biogeography

As a field of study, biogeography may be considered a bricolage - it has been constructed from many different facets from an array of research disciplines including biology, botany, zoology, geography, and geology. Biogeography focuses on the study of the constantly changing ranges of plants and animals, over multitude of space and time scales. It also includes the study of the structure and dynamics of biotic communities and ecosystems as they relate to both natural and anthropogenic processes. As it exists today, biogeography is an interdisciplinary research area founded in both the biological and Earth sciences. From a purely biological perspective, biogeography may be perceived as one of two types of studies: 1. biotic distributions and broad scales, and interpretations of the evolutionary and dispersal history of a single taxon or a few taxa; or 2. biotic distributions at local-to-regional scales, and interpretations of these distributions in relation to contemporary environments and rates of immigration or extinction. The first type of study is what is most usually associated with the term "biogeography" as disciplinary research field. It is conventionally termed "classical biogeography" because it reflects the continuity of research foci on which biogeography was founded in the nineteenth-century. The second type of biogeographical study has more modern day roots and is termed "geographical ecology" to reflect the theoretical predilections of ecologists and population biologists. Geographical ecology for all intents has become merged with ecology and exists as a sub discipline within this larger field of study.

Quattrochi, Dale A.↗

Vegetation biogeography is a main source of uncertainty in modelling the land carbon cycle

The terrestrial biosphere exchanges a large amount of CO 2 with the atmosphere through photosynthesis and respiration, determining the magnitude of land carbon sink and consequently influencing the rate of global warming. The magnitudes of global photosynthesis and respiration, however, vary widely across models (100-200 PgC/year), constituting a key and persistent source of uncertainty in carbon cycle and climate modelling. Here, we argue that the uncertainty in the land carbon cycle modelling is largely attributable to the uncertainty in biogeography – the distribution of plant functional types (PFTs). Using an ensemble of dynamic global vegetation models (DGVMs), we find a strong dependence of total photosynthesis on total area for each PFT. The dependence allows us to reduce the spread of land carbon cycle estimates by ~75% using remote sensing-based PFT maps. We further find that 56 ± 21% of climate-driven changes in global photosynthesis modelled by DGVMs are caused by changes in PFT distribution in the last two decades. Our study identifies vegetation biogeography as a main controlling factor of uncertainty in land carbon cycle modelling and highlights the importance of biogeography-climate interactions in carbon cycle and climate studies.

Zhao, Ruiying [National Univ. of Singapore (Singap↗

Genomic and environmental controls on Castellaniella biogeography in an anthropogenically disturbed subsurface

Castellaniella species have been isolated from a variety of mixed-waste environments including the nitrate and multiple metal-contaminated subsurface at the Oak Ridge Reservation (ORR). Previous studies examining microbial community composition and nitrate removal at ORR during biostimulation efforts reported increased abundances of members of the Castellaniella genus concurrent with increased denitrification rates. Thus, we asked how genomic and abiotic factors control the Castellaniella biogeography at the site to understand how these factors may influence nitrate transformation in an anthropogenically impacted setting. We report the isolation and characterization of several Castellaniella strains from the ORR subsurface. Five of these isolates match at 100% identity (at the 16S rRNA gene V4 region) to two Castellaniella amplicon sequence variants (ASVs), ASV1 and ASV2, that have persisted in the ORR subsurface for at least 2 decades. However, ASV2 has consistently higher relative abundance in samples taken from the site and was also the dominant blooming denitrifier population during a prior biostimulation effort. We found that the ASV2 representative strain has greater resistance to mixed metal stress than the ASV1 representative strains. We attribute this resistance, in part, to the large number of unique heavy metal resistance genes identified on a genomic island in the ASV2 representative genome. Additionally, we suggest that the relatively lower fitness of ASV1 may be connected to the loss of the nitrous oxide reductase (nos) operon (and associated nitrous oxide reductase activity) due to the insertion at this genomic locus of a mobile genetic element carrying copper resistance genes. This study demonstrates the value of integrating genomic, environmental, and phenotypic data to characterize the biogeography of key microorganisms in contaminated sites.

59 BASIC BIOLOGICAL SCIENCES↗

Anatomy of a mega‐radiation: Biogeography and niche evolution in Astragalus

Premise Astragalus (Fabaceae), with more than 3000 species, represents a globally successful radiation of morphologically highly similar species predominant across the northern hemisphere. It has attracted attention from systematists and biogeographers, who have asked what factors might be behind the extraordinary diversity of this important arid-adapted clade and what sets it apart from close relatives with far less species richness. Methods Here, for the first time using extensive phylogenetic sampling, we asked whether (1) Astragalus is uniquely characterized by bursts of radiation or whether diversification instead is uniform and no different from closely related taxa. Then we tested whether the species diversity of Astragalus is attributable specifically to its predilection for (2) cold and arid habitats, (3) particular soils, or to (4) chromosome evolution. Finally, we tested (5) whether Astragalus originated in central Asia as proposed and (6) whether niche evolutionary shifts were subsequently associated with the colonization of other continents. Results Our results point to the importance of heterogeneity in the diversification of Astragalus, with upshifts associated with the earliest divergences but not strongly tied to any abiotic factor or biogeographic regionalization tested here. The only potential correlate with diversification we identified was chromosome number. Biogeographic shifts have a strong association with the abiotic environment and highlight the importance of central Asia as a biogeographic gateway. Conclusions Our investigation shows the importance of phylogenetic and evolutionary studies of logistically challenging “mega-radiations.” Our findings reject any simple key innovation behind high diversity and underline the often nuanced, multifactorial processes leading to species-rich clades.

59 BASIC BIOLOGICAL SCIENCES↗

Microbial communities of Auka hydrothermal sediments shed light on vent biogeography and the evolutionary history of thermophily

Abstract Hydrothermal vents have been key to our understanding of the limits of life, and the metabolic and phylogenetic diversity of thermophilic organisms. Here we used environmental metagenomics combined with analysis of physicochemical data and 16S rRNA gene amplicons to characterize the sediment-hosted microorganisms at the recently discovered Auka vents in the Gulf of California. We recovered 325 metagenome assembled genomes (MAGs) representing 54 phyla, over 30% of those currently known, showing the microbial community in Auka hydrothermal sediments is highly diverse. 16S rRNA gene amplicon screening of 224 sediment samples across the vent field indicates that the MAGs retrieved from a single site are representative of the microbial community in the vent field sediments. Metabolic reconstruction of a vent-specific, deeply branching clade within the Desulfobacterota suggests these organisms metabolize sulfur using novel octaheme cytochrome-c proteins related to hydroxylamine oxidoreductase. Community-wide comparison between Auka MAGs and MAGs from Guaymas Basin revealed a remarkable 20% species-level overlap, suggestive of long-distance species transfer over 400 km and subsequent sediment colonization. Optimal growth temperature prediction on the Auka MAGs, and thousands of reference genomes, shows that thermophily is a trait that has evolved frequently. Taken together, our Auka vent field results offer new perspectives on our understanding of hydrothermal vent microbiology.

54 ENVIRONMENTAL SCIENCES↗

Genome-resolved biogeography of Phaeocystales, cosmopolitan bloom-forming algae

Phaeocystales, comprising the genus Phaeocystis and an uncharacterized sister lineage, are nanoplanktonic haptophytes widespread in the global ocean. Several species form mucilaginous colonies and influence key biogeochemical cycles, yet their underlying diversity and ecological strategies remain underexplored. Here, we present new genomic data from 13 strains, including three high-quality reference genomes (N50 > 30 kbp), and integrate previous metagenome-assembled genomes to resolve a robust phylogeny. Divergence timing of P. antarctica aligns with Miocene cooling and Southern Ocean isolation. Genomic traits reveal metabolic flexibility, including mixotrophic nitrogen acquisition in temperate waters and gene expansions linked to polar nutrient adaptation. Concordantly, transcriptomic comparisons between temperate and polar Phaeocystis suggest Southern Ocean populations experience iron and B12 limitation. We also identify signatures of horizontal gene transfer and endogenous giant virus/virophage insertions. Together, these findings highlight Phaeocystales as an ecologically versatile and geographically widespread lineage shaped by evolutionary innovation and adaptation to contrasting environmental stressors.

Füssy, Zoltán↗

The biogeography of soil and airborne fungi in the Southwestern USA in relation to climate and vegetation

To assess how fungal dispersal might respond to climate change, we examined how climate and geography influence the regional distribution of fungi in soil and air. Specifically, we hypothesized that neighboring fungal communities should be more similar than distant communities (i.e. spatially autocorrelated) and that fungal dispersal should be more limited in soil than in air. We collected soil and air samples from 60 sites across five states in the Southwestern USA. Then, we sequenced the ITS2 region to identify fungal taxa in each sample. Next, we used distance-based redundancy analysis to partition variation in fungal community composition between climate variables and spatial structure. Fungi were indeed spatially autocorrelated. Moreover, precipitation, maximum vapor pressure deficit, and soil moisture were significantly related to fungal community composition in soils. In comparison, only precipitation was significantly related to community composition in the air. After accounting for climate, the strength of spatial autocorrelation did not differ significantly in soilborne versus airborne fungi. Dispersal limitation was evident in soilborne fungi at short distances (<100 km) and was not observed at any distance in airborne fungi. Altogether, climate may influence which fungal taxa are present in soil and air, and fungi could feasibly wind disperse over regional scales.

54 ENVIRONMENTAL SCIENCES↗

Eukaryotic genomes from a global metagenomic data set illuminate trophic modes and biogeography of ocean plankton

ABSTRACT Metagenomics is a powerful method for interpreting the ecological roles and physiological capabilities of mixed microbial communities. Yet, many tools for processing metagenomic data are neither designed to consider eukaryotes nor are they built for an increasing amount of sequence data. EukHeist is an automated pipeline to retrieve eukaryotic and prokaryotic metagenome-assembled genomes (MAGs) from large-scale metagenomic sequence data sets. We developed the EukHeist workflow to specifically process large amounts of both metagenomic and/or metatranscriptomic sequence data in an automated and reproducible fashion. Here, we applied EukHeist to the large-size fraction data (0.8–2,000 µm) from Tara Oceans to recover both eukaryotic and prokaryotic MAGs, which we refer to as TOPAZ (Tara Oceans Particle-Associated MAGs). The TOPAZ MAGs consisted of >900 environmentally relevant eukaryotic MAGs and >4,000 bacterial and archaeal MAGs. The bacterial and archaeal TOPAZ MAGs expand upon the phylogenetic diversity of likely particle- and host-associated taxa. We use these MAGs to demonstrate an approach to infer the putative trophic mode of the recovered eukaryotic MAGs. We also identify ecological cohorts of co-occurring MAGs, which are driven by specific environmental factors and putative host-microbe associations. These data together add to a number of growing resources of environmentally relevant eukaryotic genomic information. Complementary and expanded databases of MAGs, such as those provided through scalable pipelines like EukHeist, stand to advance our understanding of eukaryotic diversity through increased coverage of genomic representatives across the tree of life. IMPORTANCE Single-celled eukaryotes play ecologically significant roles in the marine environment, yet fundamental questions about their biodiversity, ecological function, and interactions remain. Environmental sequencing enables researchers to document naturally occurring protistan communities, without culturing bias, yet metagenomic and metatranscriptomic sequencing approaches cannot separate individual species from communities. To more completely capture the genomic content of mixed protistan populations, we can create bins of sequences that represent the same organism (metagenome-assembled genomes [MAGs]). We developed the EukHeist pipeline, which automates the binning of population-level eukaryotic and prokaryotic genomes from metagenomic reads. We show exciting insight into what protistan communities are present and their trophic roles in the ocean. Scalable computational tools, like EukHeist, may accelerate the identification of meaningful genetic signatures from large data sets and complement researchers’ efforts to leverage MAG databases for addressing ecological questions, resolving evolutionary relationships, and discovering potentially novel biodiversity.

59 BASIC BIOLOGICAL SCIENCES↗

Regional biogeography versus intra-annual dynamics of the root and soil microbiome

Abstract Background Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). Results To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. Conclusions Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.

59 BASIC BIOLOGICAL SCIENCES↗

KBase Narrative - Genomic and environmental controls on Castellaniella biogeography in an anthropogenically disturbed site

Genome assemblies were imported into KBase using the Batch Import Assembly from Staging Area (v1.0.57) function. All assemblies were annotated using the Annotated Multiple Microbial Assemblies with RASTtk - v1.073 tool. Annotated genomes were grouped into sets using the Add Genomes to GenomeSet - v1.7.6 function. Individual annotated genomes can be found both below and in the Data menu to the left. Taxonomy was assigned using the Classify Microbes with GTDB-Tk-v1.7.0 tool. The results of this analysis are shown below. Analysis of the Castellaniella pangenome was performed using the Compute Pangenome (v0.0.7) tool. Using the same method, we also computed the ORR-specific and non-ORR Castellaniella pangenomes. All pangenome results (including the presence/absence matrix) can be found below.

Szink, Elizabeth↗

Using neural network ensembles to separate ocean biogeochemical and physical drivers of phytoplankton biogeography in Earth system models

Abstract. Earth system models (ESMs) are useful tools for predicting and understanding past and future aspects of the climate system. However, the biological and physical parameters used in ESMs can have wide variations in their estimates. Even small changes in these parameters can yield unexpected results without a clear explanation of how a particular outcome was reached. The standard method for estimating ESM sensitivity is to compare spatiotemporal distributions of variables from different runs of a single ESM. However, a potential pitfall of this method is that ESM output could match observational patterns because of compensating errors. For example, if a model predicts overly weak upwelling and low nutrient concentrations, it might compensate for this by allowing phytoplankton to have a high sensitivity to nutrients. Recently, we demonstrated that neural network ensembles (NNEs) are capable of extracting relationships between predictor and target variables within ocean biogeochemical models. Being able to view the relationships between variables, along with spatiotemporal distributions, allows for a more mechanistically based examination of ESM outputs. Here, we investigated whether we could apply NNEs to help us determine why different ESMs produce different spatiotemporal distributions of phytoplankton biomass. We tested this using three cases. The first and second case used different runs of the same ESM, except that the physical circulations differed between them in the first case, while the biological equations differed between them in the second. Our results indicated that the NNEs were capable of extracting the relationships between variables for different runs of a single ESM, allowing us to distinguish between differences due to changes in circulation (which do not change relationships) from changes in biogeochemical formulation (which do change relationships). In the third case, we applied NNEs to two different ESMs. The results of the third case highlighted the capability of NNEs to contrast the apparent relationships of different ESMs and some of the challenges it presents. Although applied specifically to the ocean components of an ESM, our study demonstrates that Earth system modelers can use NNEs to separate the contributions of different components of ESMs. Specifically, this allows modelers to compare the apparent relationships across different ESMs and observational datasets.

54 ENVIRONMENTAL SCIENCES↗

The historic biogeography of India: isolation or contact?

Geophysical maps depicting continental movement have consistently shown India, as it moved northward, to be located far out in the Tethys Sea. India split off from the African east coast about 148 m.y.a. From that time onward, according to almost all geophysical accounts, India was isolated from all of other continents until the early Miocene when it made contact with Eurasia. But the biological data, both fossil and Recent, indicate that this concept cannot be correct. If India had really existed as an isolated, oceanic continent for about 100 m.y., it should have developed a peculiar biota with many endemic genera and families in its terrestrial and shallow marine habitats. But there are virtually no remains of organisms indicating that India was isolated for any substantial time (millions of years). Instead, we find that almost all Indian taxa were possessed in common with other continents. As time went on, the northern relationships became stronger and the southern ones weaker. Most of the recent geophysical accounts show India not making contact with Eurasia until the early Miocene, but fossil materials show that this event must have taken place by the early Eocene. It has been postulated that, as India moved northward, it created a biogeographic barrier that separated marine fish populations and resulted in the east-west provinces that are now apparent in the Indian Ocean. At the same time, the barrier effect was supposed to have resulted in the formation of sister species that are now located far apart. Information currently available indicates that most living, tropical marine species are probably not over 3 m.y. old. Consequently, the northward movement of India, which took place primarily between 148 and 50 m.y.a., could have no bearing on the relationships of modern species.

NASA Discipline Exobiology↗

Quantitative Measures of Immersion in Cloud and the Biogeography of Cloud Forests

Sites described as tropical montane cloud forests differ greatly, in part because observers tend to differ in their opinion as to what constitutes frequent and prolonged immersion in cloud. This definitional difficulty interferes with hydrologic analyses, assessments of environmental impacts on ecosystems, and biogeographical analyses of cloud forest communities and species. Quantitative measurements of cloud immersion can be obtained on site, but the observations are necessarily spatially limited, although well-placed observers can examine 10 50 km of a mountain range under rainless conditions. Regional analyses, however, require observations at a broader scale. This chapter discusses remote sensing and modeling approaches that can provide quantitative measures of the spatiotemporal patterns of cloud cover and cloud immersion in tropical mountain ranges. These approaches integrate remote sensing tools of various spatial resolutions and frequencies of observation, digital elevation models, regional atmospheric models, and ground-based observations to provide measures of cloud cover, cloud base height, and the intersection of cloud and terrain. This combined approach was applied to the Monteverde region of northern Costa Rica to illustrate how the proportion of time the forest is immersed in cloud may vary spatially and temporally. The observed spatial variation was largely due to patterns of airflow over the mountains. The temporal variation reflected the diurnal rise and fall of the orographic cloud base, which was influenced in turn by synoptic weather conditions, the seasonal movement of the Intertropical Convergence Zone and the north-easterly trade winds. Knowledge of the proportion of the time that sites are immersed in clouds should facilitate ecological comparisons and biogeographical analyses, as well as land use planning and hydrologic assessments in areas where intensive on-site work is not feasible.

Lawton, R. O.↗

Increasing Threat of Wildfires: the Year 2020 in Perspective: A Global Ecology and Biogeography Special Issue

Each year, wild and managed fires burn roughly 4 million km2 [~400 million hectares (Mha)] of savanna, forest, grassland and agricultural ecosystems. Land use and climate change have altered fire regimes throughout the world, with a trend toward higher-severity fires found from Australia, the Americas, Europe and Asia, to the Arctic. In 2020, there were notable catastrophic fires in Australia (in the 2019/20 Austral fire season), the Western United States, South America and Siberia. These fires defined much of the global fire year and were compounded by the socio-economic disruption of the Coronavirus 2019 (COVID-19) pandemic.

Rachael H Nolan↗