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

2020 ◽  
Vol 14 (10) ◽  
pp. 2595-2609 ◽  
Author(s):  
Wei Qin ◽  
Yue Zheng ◽  
Feng Zhao ◽  
Yulin Wang ◽  
Hidetoshi Urakawa ◽  
...  

Abstract 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.

2020 ◽  
Author(s):  
Baozhan Wang ◽  
Wei Qin

<p>The membrane rotary energy-yielding ATPases represent the cornerstone of cellular bioenergetics for all three domains of life. The archaeal ATPases (A-type ATPases) are functionally similar to the eukaryotic and bacterial F-type ATPases that catalyze ATP synthesis using a PMF. However, they are structurally more similar to the vacuolar-type (V-type) ATPases of eukaryotes and some bacteria that function as proton pumps driven by ATP hydrolysis. Significant variation in subunit composition, structure, and mechanism of the archaeal ATPases is thought to confer adaptive advantage in the variety of extreme environments that archaea inhabit.</p><p>The ammonia-oxidizing archaea are recognized to exert primary control of nitrification in the marine environment, are major contributors to soil nitrification, and have a habitat range extending from geothermal systems, to acidic soils and the oceanic abyss. The basis for their remarkable adaptive radiation is obscured by a relatively simple metabolism – autotrophic growth using ammonia for energy and nitrogen. In this study, we find that their adaptation to acidic habitats and the extreme pressures of the hadal zone of the ocean at depths below 6000 meters is correlated with horizontal transfer of a variant of the energy-yielding ATPase (atp) operon. Whereas the ATPase genealogy of neutrophilic soil and upper ocean pelagic AOA is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically disparate clades of acidophilic and piezophilic species.</p><p>A function of the so-acquired V-ATPases in pumping excessive cytoplasmic protons at low pH is consistent with its increased expression by acid-tolerant AOA with decreasing pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E.coli at low pH. Additional support for adaptive significance derives from our observation that horizontal transfer is also associated with the adaptive radiation of Micrarchaeota, Parvarchaeota and Marsarchaeota into acidic environments. Their ATPases are affiliated with the acidophilic lineage ATPases of Thermoplasmatales and phylogenetically divergent from the corresponding species tree.</p><p>Another notable finding is that single hadopelagic AOA species contain both A- and V-type ATPases, suggesting that extensive horizontal transfer of atp operons is a highly active and ongoing process within AOA. The presence of an additional V-type ATPase in hadopelagic AOA may provide fitness advantages in the deep ocean with elevated hydrostatic pressure, as the proposed function of V-ATPase in pumping excessive cytoplasmic protons at high pressure may serve to maintain the cytosolic pH homeostasis in marine AOA.</p><p>Taken together, our study provides the first clear evidence of a significant role of horizontal transfer of atp operon in the adaptive radiation of AOA, one of the most successful organisms on Earth, and other archaeal species, spanning the TACK and DPANN superphyla as well as Euryarchaeota phylum.</p>


2019 ◽  
Vol 21 (2) ◽  
pp. 716-729 ◽  
Author(s):  
Yong Wang ◽  
Jiao-Mei Huang ◽  
Guo-Jie Cui ◽  
Takuro Nunoura ◽  
Yoshihiro Takaki ◽  
...  

Geology ◽  
2021 ◽  
Author(s):  
Adam D. McArthur ◽  
Daniel E. Tek

The type and volume of sediment entering subduction zones affects the style of plate-boundary deformation and thus sedimentary and tectonic cycles. Because submarine channels significantly increase the transport efficiency of turbidity currents, their presence or absence in subduction trenches is a primary control on trench fill. To date, comprehensive architectural characterization of trench-axial channels has not been possible, undermining efforts to identify the factors controlling their initiation and evolution. Here, we describe the evolution of the Hikurangi Channel, which traverses the Hikurangi Trench, offshore New Zealand. Analysis of two- and three-dimensional seismic data reveals that the channel was present only during the last ~3.5 m.y. of the ~27 m.y. of the trench’s existence; its inception and propagation resulted from increased sediment supply to the trench following amplified hinterland exhumation. To test if the controls on the evolution of the Hikurangi Channel are universal, multivariate statistical analysis of the geomorphology of subduction trenches globally is used to investigate the formative conditions of axial channels in modern trenches. Terrigenous sediment supply and thickness of sediment cover in a trench are the dominant controls; subsidiary factors such as trench length and rugosity also contribute to the conditions necessary for trench-axial channel development. Axial channels regulate sediment distribution in trenches, and this varies temporally and spatially as a channel propagates along a trench. The presence of a trench-axial channel affects plate-boundary mechanics and has implications for the style of subduction-margin deformation.


2016 ◽  
Vol 113 (28) ◽  
pp. 7888-7893 ◽  
Author(s):  
Jong-Geol Kim ◽  
Soo-Je Park ◽  
Jaap S. Sinninghe Damsté ◽  
Stefan Schouten ◽  
W. Irene C. Rijpstra ◽  
...  

Ammonia-oxidizing archaea (AOA), that is, members of the Thaumarchaeota phylum, occur ubiquitously in the environment and are of major significance for global nitrogen cycling. However, controls on cell growth and organic carbon assimilation by AOA are poorly understood. We isolated an ammonia-oxidizing archaeon (designated strain DDS1) from seawater and used this organism to study the physiology of ammonia oxidation. These findings were confirmed using four additional Thaumarchaeota strains from both marine and terrestrial habitats. Ammonia oxidation by strain DDS1 was enhanced in coculture with other bacteria, as well as in artificial seawater media supplemented with α-keto acids (e.g., pyruvate, oxaloacetate). α-Keto acid-enhanced activity of AOA has previously been interpreted as evidence of mixotrophy. However, assays for heterotrophic growth indicated that incorporation of pyruvate into archaeal membrane lipids was negligible. Lipid carbon atoms were, instead, derived from dissolved inorganic carbon, indicating strict autotrophic growth. α-Keto acids spontaneously detoxify H2O2 via a nonenzymatic decarboxylation reaction, suggesting a role of α-keto acids as H2O2 scavengers. Indeed, agents that also scavenge H2O2, such as dimethylthiourea and catalase, replaced the α-keto acid requirement, enhancing growth of strain DDS1. In fact, in the absence of α-keto acids, strain DDS1 and other AOA isolates were shown to endogenously produce H2O2 (up to ∼4.5 μM), which was inhibitory to growth. Genomic analyses indicated catalase genes are largely absent in the AOA. Our results indicate that AOA broadly feature strict autotrophic nutrition and implicate H2O2 as an important factor determining the activity, evolution, and community ecology of AOA ecotypes.


Author(s):  
Frank O. Aylward ◽  
Alyson E. Santoro

AbstractThe Thaumarchaeota comprise a diverse archaeal phylum including numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically-characterized marine Thaumarchaeota are reported to be chemolithoautotrophic ammonia-oxidizers. In this study, we report a group of heterotrophic marine Thaumarchaeota (HMT) with ultrasmall genome sizes that is globally abundant in deep ocean waters, apparently lacking the ability to oxidize ammonia. We assemble five HMT genomes from metagenomic data derived from both the Atlantic and Pacific Oceans, including two that are >95% complete, and show that they form a deeply-branching lineage sister to the ammonia-oxidizing archaea (AOA). Metagenomic read mapping demonstrates the presence of this group in mesopelagic samples from all major ocean basins, with abundances reaching up to 6% that of AOA. Surprisingly, the predicted sizes of complete HMT genomes are only 837-908 Kbp, 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 highly reduced metabolism for aerobic heterotrophy that, although lacking the carbon fixation pathway typical of AOA, includes a divergent form III-a RuBisCO that potentially functions in a nucleotide scavenging pathway. Despite the small genome size of this group, we identify 13 encoded pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to shuttle reducing equivalents to the electron transport chain, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations.ImportanceIt 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 heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from 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 generate 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.


2021 ◽  
Author(s):  
Torda Varga ◽  
Csenge Földi ◽  
Viktória Bense ◽  
László G. Nagy

AbstractFungi evolved complex fruiting body (‘mushroom’) morphologies as adaptations to efficient spore dispersal in terrestrial habitats. Mushroom-forming fungi (Agaricomycetes) display a graded series of developmental innovations related to fruiting body morphology, however, how these evolved is largely unknown, leaving the functional biology and evolutionary principles of complex multicellularity in the third largest multicellular kingdom poorly known. Here, we show that developmental innovations of mushroom-forming fungi that enclose the spore-producing surface (hymenophore) in a protected environment display significant asymmetry in their evolution and are associated with increased diversification rates. ‘Enclosed’ development and related tissues (partial and universal veils) evolved convergently and became a widespread developmental type in clades in which it emerged. This probably mirrors increased fitness for protected fruiting body initials in terrestrial habitats, by better coping with environmental factors such as desiccation or predators, among others. We observed similar patterns in the evolution of complex hymenophore architectures, such as gills, pores or teeth, which optimize biomass-to-propagule number ratios and were found to spur diversification in mushrooms. Taken together, our results highlight new morphological traits associated with the adaptive radiation of mushroom-forming fungi and present formal phylogenetic testing of hypotheses on the reproductive ecology of a poorly known but hyperdiverse clade.


2021 ◽  
Vol 288 (1953) ◽  
pp. 20210340
Author(s):  
Steven Poe ◽  
Lorenzo A. H. Donald ◽  
Christopher Anderson

Adaptive radiations fill ecological and morphological space during evolutionary diversification. Why do some trait combinations evolve during such radiations, whereas others do not? ‘Required’ constraints of pleiotropy and developmental interaction frequently are implicated in explanations for such patterns, but selective forces also may discourage particular trait combinations. Here, we use a dataset of 351 species to demonstrate the dearth of some theoretically plausible trait combinations of limb, toe and tail length in Anolis lizards. For example, disproportionately few Anolis species display long limbs and short toes. We evaluate recovered patterns within three species of Anolis , and find that cladewide patterns are not evident at intraspecific levels. For example, within species, the combination of long limbs and short toes is not significantly rarer than long limbs and long toes. Differences in scale complicate inter- and intraspecific comparisons and disallow concrete conclusions of cause. However, the absence of the interspecific pattern at the intraspecific level is more compatible with selection favouring particular trait combinations than with ‘required’ forces dictating which trait combinations are available for selection. We also demonstrate the isometry of toe, tail and hindlimb length relative to body length between species but allometry in four of nine trait–body comparisons within species.


2021 ◽  
Vol 12 ◽  
Author(s):  
Li Liu ◽  
Daniel M. Schubert ◽  
Martin Könneke ◽  
Ivan A. Berg

Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant organisms that exert primary control of oceanic and soil nitrification and are responsible for a large part of dark ocean primary production. They assimilate inorganic carbon via an energetically efficient version of the 3-hydroxypropionate/4-hydroxybutyrate cycle. In this cycle, acetyl-CoA is carboxylated to succinyl-CoA, which is then converted to two acetyl-CoA molecules with 4-hydroxybutyrate as the key intermediate. This conversion includes the (S)-3-hydroxybutyryl-CoA dehydrogenase reaction. Here, we heterologously produced the protein Nmar_1028 catalyzing this reaction in thaumarchaeon Nitrosopumilus maritimus, characterized it biochemically and performed its phylogenetic analysis. This NAD-dependent dehydrogenase is highly active with its substrate, (S)-3-hydroxybutyryl-CoA, and its low Km value suggests that the protein is adapted to the functioning in the 3-hydroxypropionate/4-hydroxybutyrate cycle. Nmar_1028 is homologous to the dehydrogenase domain of crotonyl-CoA hydratase/(S)-3-hydroxybutyryl-CoA dehydrogenase that is present in many Archaea. Apparently, the loss of the dehydratase domain of the fusion protein in the course of evolution was accompanied by lateral gene transfer of 3-hydroxypropionyl-CoA dehydratase/crotonyl-CoA hydratase from Bacteria. Although (S)-3-hydroxybutyryl-CoA dehydrogenase studied here is neither unique nor characteristic for the HP/HB cycle, Nmar_1028 appears to be the only (S)-3-hydroxybutyryl-CoA dehydrogenase in N. maritimus and is thus essential for the functioning of the 3-hydroxypropionate/4-hydroxybutyrate cycle and for the biology of this important marine archaeon.


Author(s):  
Peter Khooshabeh ◽  
Mary Hegarty ◽  
Thomas F. Shipley

Two experiments tested the hypothesis that imagery ability and figural complexity interact to affect the choice of mental rotation strategies. Participants performed the Shepard and Metzler (1971) mental rotation task. On half of the trials, the 3-D figures were manipulated to create “fragmented” figures, with some cubes missing. Good imagers were less accurate and had longer response times on fragmented figures than on complete figures. Poor imagers performed similarly on fragmented and complete figures. These results suggest that good imagers use holistic mental rotation strategies by default, but switch to alternative strategies depending on task demands, whereas poor imagers are less flexible and use piecemeal strategies regardless of the task demands.


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