An AAA+ ATPase Clamshell Targets Transposition.

DNA transposition plays key roles in genome diversity, pathogenesis, and evolution. Yet, structural and mechanistic information on transposition targeting and regulation is limited. Arias-Palomo and Berger now define the decameric organization of the AAA+ ATPase IstB, unveiling key insights into its targeting and regulation of IstA transposase activity.

Coral reefs benefit from reduced land-sea impacts under ocean warming.

Coral reef ecosystems are being fundamentally restructured by local human impacts and climate-driven marine heatwaves that trigger mass coral bleaching and mortality1. Reducing local impacts can increase reef resistance to and recovery from bleaching2. However, resource managers lack clear advice on targeted actions that best support coral reefs under climate change3 and sector-based governance means most land- and sea-based management efforts remain siloed4. Here we combine surveys of reef change with a unique 20-year time series of land-sea human impacts that encompassed an unprecedented marine heatwave in Hawai'i. Reefs with increased herbivorous fish populations and reduced land-based impacts, such as wastewater pollution and urban runoff, had positive coral cover trajectories predisturbance. These reefs also experienced a modest reduction in coral mortality following severe heat stress compared to reefs with reduced fish populations and enhanced land-based impacts. Scenario modelling indicated that simultaneously reducing land-sea human impacts results in a three- to sixfold greater probability of a reef having high reef-builder cover four years postdisturbance than if either occurred in isolation. International efforts to protect 30% of Earth's land and ocean ecosystems by 2030 are underway5. Our results reveal that integrated land-sea management could help achieve coastal ocean conservation goals and provide coral reefs with the best opportunity to persist in our changing climate.

ATM phosphorylates the FATC domain of DNA-PKcs at threonine 4102 to promote non-homologous end joining.

Ataxia-telangiectasia mutated (ATM) drives the DNA damage response via modulation of multiple signal transduction and DNA repair pathways. Previously, ATM activity was implicated in promoting the non-homologous end joining (NHEJ) pathway to repair a subset of DNA double-stranded breaks (DSBs), but how ATM performs this function is still unclear. In this study, we identified that ATM phosphorylates the DNA-dependent protein kinase catalytic subunit (DNA-PKcs), a core NHEJ factor, at its extreme C-terminus at threonine 4102 (T4102) in response to DSBs. Ablating phosphorylation at T4102 attenuates DNA-PKcs kinase activity and this destabilizes the interaction between DNA-PKcs and the Ku-DNA complex, resulting in decreased assembly and stabilization of the NHEJ machinery at DSBs. Phosphorylation at T4102 promotes NHEJ, radioresistance, and increases genomic stability following DSB induction. Collectively, these findings establish a key role for ATM in NHEJ-dependent repair of DSBs through positive regulation of DNA-PKcs.

Variation in farming damselfish behaviour creates a competitive landscape of risk on coral reefs.

Interspecific interactions are fundamental drivers of animal space use. Yet while non-consumptive effects of predation risk on prey space use are well-known, the risk of aggressive interactions on space use of competitors is largely unknown. We apply the landscape of risk framework to competition-driven space use for the first time, with the hypothesis that less aggressive competitors may alter their behaviour to avoid areas of high competitor density. Specifically, we test how aggressive risk from territorial algal-farming damselfishes can shape the spatial distribution of herbivore fish competitors. We found that only the most aggressive damselfish had fewer competitors in their surrounding area, demonstrating that individual-level behavioural variation can shape spatial distributions. In contradiction to the landscape of risk framework, abundances of farming damselfish and other fishes were positively associated. Our results suggest that reef fishes do not simply avoid areas of high damselfish abundance, but that spatial variation in aggressive behaviour, rather than of individuals, created a competitive landscape of risk. We emphasize the importance of individual-level behaviour in identifying patterns of space use and propose expanding the landscape of risk framework to non-predatory interactions to explore cascading behavioural responses to aggressive risk.

Influence of upwelling on coral reef benthic communities: a systematic review and meta-analysis.

Highly competitive coral reef benthic communities are acutely sensitive to changes in environmental parameters such as temperature and nutrient concentrations. Physical oceanographic processes that induce upwelling therefore act as drivers of community structure on tropical reefs. How upwelling impacts coral communities, however, is not fully understood; upwelling may provide a natural buffer against climate impacts and could potentially enhance the efficacy of spatial management and reef conservation efforts. This study employed a systematic review to assess existing literature linking upwelling with reef community structure, and a meta-analysis to quantify upwelling impact on the percentage cover of coral reef benthic groups. We show that upwelling has context-dependant effects on the cover of hard coral and fleshy macroalgae, with effect size and direction varying with depth, region and remoteness. Fleshy macroalgae were found to increase by 110% on inhabited reefs yet decrease by 56% around one well-studied remote island in response to upwelling. Hard coral cover was not significantly impacted by upwelling on inhabited reefs but increased by 150% when direct local human pressures were absent. By synthesizing existing evidence, this review facilitates adaptive and nuanced reef management which considers the influence of upwelling on reef assemblages.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

A charged performance by gp17 in viral packaging.

Packaging of viral genomes into virus capsids requires powerful motors to overcome the repulsive force that builds as the nucleic acids are compressed. Through structural analyses of the T4 bacteriophage packaging motor gp17, Sun et al. (2008) now propose a packaging mechanism in which electrostatic forces cause the motor to alternate between tensed and relaxed conformational states.

Prey-size plastics are invading larval fish nurseries.

Life for many of the world's marine fish begins at the ocean surface. Ocean conditions dictate food availability and govern survivorship, yet little is known about the habitat preferences of larval fish during this highly vulnerable life-history stage. Here we show that surface slicks, a ubiquitous coastal ocean convergence feature, are important nurseries for larval fish from many ocean habitats at ecosystem scales. Slicks had higher densities of marine phytoplankton (1.7-fold), zooplankton (larval fish prey; 3.7-fold), and larval fish (8.1-fold) than nearby ambient waters across our study region in Hawai'i. Slicks contained larger, more well-developed individuals with competent swimming abilities compared to ambient waters, suggesting a physiological benefit to increased prey resources. Slicks also disproportionately accumulated prey-size plastics, resulting in a 60-fold higher ratio of plastics to larval fish prey than nearby waters. Dissections of hundreds of larval fish found that 8.6% of individuals in slicks had ingested plastics, a 2.3-fold higher occurrence than larval fish from ambient waters. Plastics were found in 7 of 8 families dissected, including swordfish (Xiphiidae), a commercially targeted species, and flying fish (Exocoetidae), a principal prey item for tuna and seabirds. Scaling up across an ∼1,000 km2 coastal ecosystem in Hawai'i revealed slicks occupied only 8.3% of ocean surface habitat but contained 42.3% of all neustonic larval fish and 91.8% of all floating plastics. The ingestion of plastics by larval fish could reduce survivorship, compounding threats to fisheries productivity posed by overfishing, climate change, and habitat loss.

Artificial shorelines lack natural structural complexity across scales.

From microbes to humans, habitat structural complexity plays a direct role in the provision of physical living space, and increased complexity supports higher biodiversity and ecosystem functioning across biomes. Coastal development and the construction of artificial shorelines are altering natural landscapes as humans seek socio-economic benefits and protection from coastal storms, flooding and erosion. In this study, we evaluate how much structural complexity is missing on artificial coastal structures compared to natural rocky shorelines, across a range of spatial scales from 1 mm to 10 s of m, using three remote sensing platforms (handheld camera, terrestrial laser scanner and uncrewed aerial vehicles). Natural shorelines were typically more structurally complex than artificial ones and offered greater variation between locations. However, our results varied depending on the type of artificial structure and the scale at which complexity was measured. Seawalls were deficient at all scales (approx. 20-40% less complex than natural shores), whereas rock armour was deficient at the smallest and largest scales (approx. 20-50%). Our findings reinforce concerns that hardening shorelines with artificial structures simplifies coastlines at organism-relevant scales. Furthermore, we offer much-needed insight into how structures might be modified to more closely capture the complexity of natural rocky shores that support biodiversity.

Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics.

Superfamily ATPases in type IV pili, type 2 secretion, and archaella (formerly archaeal flagella) employ similar sequences for distinct biological processes. Here, we structurally and functionally characterize prototypical superfamily ATPase FlaI in Sulfolobus acidocaldarius, showing FlaI activities in archaeal swimming-organelle assembly and movement. X-ray scattering data of FlaI in solution and crystal structures with and without nucleotide reveal a hexameric crown assembly with key cross-subunit interactions. Rigid building blocks form between N-terminal domains (points) and neighboring subunit C-terminal domains (crown ring). Upon nucleotide binding, these six cross-subunit blocks move with respect to each other and distinctly from secretion and pilus ATPases. Crown interactions and conformations regulate assembly, motility, and force direction via a basic-clamp switching mechanism driving conformational changes between stable, backbone-interconnected moving blocks. Collective structural and mutational results identify in vivo functional components for assembly and motility, phosphate-triggered rearrangements by ATP hydrolysis, and molecular predictors for distinct ATPase superfamily functions.

Three-dimensional digital mapping of ecosystems: a new era in spatial ecology.

Ecological processes occur over multiple spatial, temporal and thematic scales in three-dimensional (3D) ecosystems. Characterizing and monitoring change in 3D structure at multiple scales is challenging within the practical constraints of conventional ecological tools. Remote sensing from satellites and crewed aircraft has revolutionized broad-scale spatial ecology, but fine-scale patterns and processes operating at sub-metre resolution have remained understudied over continuous extents. We introduce two high-resolution remote sensing tools for rapid and accurate 3D mapping in ecology-terrestrial laser scanning and structure-from-motion photogrammetry. These technologies are likely to become standard sampling tools for mapping and monitoring 3D ecosystem structure across currently under-sampled scales. We present practical guidance in the use of the tools and address barriers to widespread adoption, including testing the accuracy of structure-from-motion models for ecologists. We aim to highlight a new era in spatial ecology that uses high-resolution remote sensing to interrogate 3D digital ecosystems.

Meta-mass shift chemical profiling of metabolomes from coral reefs.

Untargeted metabolomics of environmental samples routinely detects thousands of small molecules, the vast majority of which cannot be identified. Meta-mass shift chemical (MeMSChem) profiling was developed to identify mass differences between related molecules using molecular networks. This approach illuminates metabolome-wide relationships between molecules and the putative chemical groups that differentiate them (e.g., H2, CH2, COCH2). MeMSChem profiling was used to analyze a publicly available metabolomic dataset of coral, algal, and fungal mat holobionts (i.e., the host and its associated microbes and viruses) sampled from some of Earth's most remote and pristine coral reefs. Each type of holobiont had distinct mass shift profiles, even when the analysis was restricted to molecules found in all samples. This result suggests that holobionts modify the same molecules in different ways and offers insights into the generation of molecular diversity. Three genera of stony corals had distinct patterns of molecular relatedness despite their high degree of taxonomic relatedness. MeMSChem profiles also partially differentiated between individuals, suggesting that every coral reef holobiont is a potential source of novel chemical diversity.

Parsing human and biophysical drivers of coral reef regimes.

Coral reefs worldwide face unprecedented cumulative anthropogenic effects of interacting local human pressures, global climate change and distal social processes. Reefs are also bound by the natural biophysical environment within which they exist. In this context, a key challenge for effective management is understanding how anthropogenic and biophysical conditions interact to drive distinct coral reef configurations. Here, we use machine learning to conduct explanatory predictions on reef ecosystems defined by both fish and benthic communities. Drawing on the most spatially extensive dataset available across the Hawaiian archipelago-20 anthropogenic and biophysical predictors over 620 survey sites-we model the occurrence of four distinct reef regimes and provide a novel approach to quantify the relative influence of human and environmental variables in shaping reef ecosystems. Our findings highlight the nuances of what underpins different coral reef regimes, the overwhelming importance of biophysical predictors and how a reef's natural setting may either expand or narrow the opportunity space for management interventions. The methods developed through this study can help inform reef practitioners and hold promises for replication across a broad range of ecosystems.

Red Sea SAR11 and Prochlorococcus Single-Cell Genomes Reflect Globally Distributed Pangenomes.

Evidence suggests many marine bacteria are cosmopolitan, with widespread but sparse strains poised to seed abundant populations under conducive growth conditions. However, studies supporting this "microbial seed bank" hypothesis have analyzed taxonomic marker genes rather than whole genomes/metagenomes, leaving open the possibility that disparate ocean regions harbor endemic gene content. The Red Sea is isolated geographically from the rest of the ocean and has a combination of high irradiance, high temperature, and high salinity that is unique among the oceans; we therefore asked whether it harbors endemic gene content. We sequenced and assembled single-cell genomes of 21 SAR11 (subclades Ia, Ib, Id, and II) and 5 Prochlorococcus (ecotype HLII) samples from the Red Sea and combined them with globally sourced reference genomes to cluster genes into ortholog groups (OGs). Ordination of OG composition could distinguish clades, including phylogenetically cryptic Prochlorococcus ecotypes LLII and LLIII. Compared with reference genomes, 1% of Prochlorococcus and 17% of SAR11 OGs were unique to the Red Sea genomes (RS-OGs). Most (83%) RS-OGs had no annotated function, but 65% of RS-OGs were expressed in diel Red Sea metatranscriptomes, suggesting they are functional. Searching Tara Oceans metagenomes, RS-OGs were as likely to be found as non-RS-OGs; nevertheless, Red Sea and other warm samples could be distinguished from cooler samples using the relative abundances of OGs. The results suggest that the prevalence of OGs in these surface ocean bacteria is largely cosmopolitan, with differences in population metagenomes manifested by differences in relative abundance rather than complete presence/absence of OGs.IMPORTANCE Studies have shown that as we sequence seawater from a selected environment deeper and deeper, we approach finding every bacterial taxon known for the ocean as a whole. However, such studies have focused on taxonomic marker genes rather than on whole genomes, raising the possibility that the lack of endemism results from the method of investigation. We took a geographically isolated water body, the Red Sea, and sequenced single cells from it. We compared those single-cell genomes to available genomes from around the ocean and to ocean-spanning metagenomes. We showed that gene ortholog groups found in Red Sea genomes but not in other genomes are nevertheless common across global ocean metagenomes. These results suggest that Baas Becking's hypothesis "everything is everywhere, but the environment selects" also applies to gene ortholog groups. This widely dispersed functional diversity may give oceanic microbial communities the functional capacity to respond rapidly to changing conditions.

Foraging consistency of coral reef fishes across environmental gradients in the central Pacific.

We take advantage of a natural gradient of human exploitation and oceanic primary production across five central Pacific coral reefs to examine foraging patterns in common coral reef fishes. Using stomach content and stable isotope (δ15N and δ13C) analyses, we examined consistency across islands in estimated foraging patterns. Surprisingly, species within the piscivore-invertivore group exhibited the clearest pattern of foraging consistency across all five islands despite there being a considerable difference in mean body mass (14 g-1.4 kg) and prey size (0.03-3.8 g). In contrast, the diets and isotopic values of the grazer-detritivores varied considerably and exhibited no consistent patterns across islands. When examining foraging patterns across environmental contexts, we found that δ15N values of species of piscivore-invertivore and planktivore closely tracked gradients in oceanic primary production; again, no comparable patterns existed for the grazer-detritivores. The inter-island consistency in foraging patterns within the species of piscivore-invertivore and planktivore and the lack of consistency among species of grazer-detritivores suggests a linkage to different sources of primary production among reef fish functional groups. Our findings suggest that piscivore-invertivores and planktivores are likely linked to well-mixed and isotopically constrained allochthonous oceanic primary production, while grazer-detritivores are likely linked to sources of benthic primary production and autochthonous recycling. Further, our findings suggest that species of piscivore-invertivore, independent of body size, converge toward consuming low trophic level prey, with a hypothesized result of reducing the number of steps between trophic levels and increasing the trophic efficiency at a community level.

ATP-driven Rad50 conformations regulate DNA tethering, end resection, and ATM checkpoint signaling.

The Mre11-Rad50 complex is highly conserved, yet the mechanisms by which Rad50 ATP-driven states regulate the sensing, processing and signaling of DNA double-strand breaks are largely unknown. Here we design structure-based mutations in Pyrococcus furiosus Rad50 to alter protein core plasticity and residues undergoing ATP-driven movements within the catalytic domains. With this strategy we identify Rad50 separation-of-function mutants that either promote or destabilize the ATP-bound state. Crystal structures, X-ray scattering, biochemical assays, and functional analyses of mutant PfRad50 complexes show that the ATP-induced 'closed' conformation promotes DNA end binding and end tethering, while hydrolysis-induced opening is essential for DNA resection. Reducing the stability of the ATP-bound state impairs DNA repair and Tel1 (ATM) checkpoint signaling in Schizosaccharomyces pombe, double-strand break resection in Saccharomyces cerevisiae, and ATM activation by human Mre11-Rad50-Nbs1 in vitro, supporting the generality of the P. furiosus Rad50 structure-based mutational analyses. These collective results suggest that ATP-dependent Rad50 conformations switch the Mre11-Rad50 complex between DNA tethering, ATM signaling, and 5' strand resection, revealing molecular mechanisms regulating responses to DNA double-strand breaks.

Achieving fidelity in homologous recombination despite extreme complexity: informed decisions by molecular profiling.

In this issue of Molecular Cell, Savir and Tlusty (2010) apply signal detection theory to show that homologous recombination machinery is optimally tuned to find homologous DNA sequences within an exceptionally high background of heterologous sequences.

Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors.

Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.

Natural bounds on herbivorous coral reef fishes.

Humans are an increasingly dominant driver of Earth's biological communities, but differentiating human impacts from natural drivers of ecosystem state is crucial. Herbivorous fish play a key role in maintaining coral dominance on coral reefs, and are widely affected by human activities, principally fishing. We assess the relative importance of human and biophysical (habitat and oceanographic) drivers on the biomass of five herbivorous functional groups among 33 islands in the central and western Pacific Ocean. Human impacts were clear for some, but not all, herbivore groups. Biomass of browsers, large excavators, and of all herbivores combined declined rapidly with increasing human population density, whereas grazers, scrapers, and detritivores displayed no relationship. Sea-surface temperature had significant but opposing effects on the biomass of detritivores (positive) and browsers (negative). Similarly, the biomass of scrapers, grazers, and detritivores correlated with habitat structural complexity; however, relationships were group specific. Finally, the biomass of browsers and large excavators was related to island geomorphology, both peaking on low-lying islands and atolls. The substantial variability in herbivore populations explained by natural biophysical drivers highlights the need for locally appropriate management targets on coral reefs.

Mechanistic insights into the role of Hop2-Mnd1 in meiotic homologous DNA pairing.

The Hop2-Mnd1 complex functions with the DMC1 recombinase in meiotic recombination. Hop2-Mnd1 stabilizes the DMC1-single-stranded DNA (ssDNA) filament and promotes the capture of the double-stranded DNA partner by the recombinase filament to assemble the synaptic complex. Herein, we define the action mechanism of Hop2-Mnd1 in DMC1-mediated recombination. Small angle X-ray scattering analysis and electron microscopy reveal that the heterodimeric Hop2-Mnd1 is a V-shaped molecule. We show that the protein complex harbors three distinct DNA binding sites, and determine their functional relevance. Specifically, the N-terminal double-stranded DNA binding functions of Hop2 and Mnd1 co-operate to mediate synaptic complex assembly, whereas ssDNA binding by the Hop2 C-terminus helps stabilize the DMC1-ssDNA filament. A model of the Hop2-Mnd1-DMC1-ssDNA ensemble is proposed to explain how it mediates homologous DNA pairing in meiotic recombination.