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Oxygen-sensing mechanisms across eukaryotic kingdoms and their roles in complex multicellularity

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Origins and evolution of hypoxia response

In our current oxygen-rich atmosphere, the ability of eukaryotic cells to sense variation in oxygen concentrations is essential for adapting to low-oxygen conditions. However, Earth’s atmosphere has not always contained such high oxygen concentrations. Hammarlund et al. discuss oxygen-sensing systems across both plants and animals and argue that the systems are functionally convergent and that their emergence in an initially hypoxic environment shaped how they operate today.

Science, this issue p. eaba3512

Structured Abstract

BACKGROUND

Animals and land plants are the most diverse complex multicellular life-forms on Earth, and their success intricately links a capacity for adhering cells to perform different tasks at different times. The performance of cell tasks, however, can be both dependent on and challenged by oxygen. Oxygen acts as the final electron acceptor for aerobic respiration but also participates in reactions to generate metabolites and structural macromolecules; recently, oxygen also has come to the fore for its signaling role in developmental programs in animals and plants. Today, the relative oxygen concentration within multicellular organisms integrates information about cell position, metabolic state, and environmental conditions. For the rise of complex life, the capacity to link oxygen perception to transcriptional responses would have allowed organisms to attune cell fates to fluctuations in oxygen availability and metabolic needs in a spatiotemporal manner.

ADVANCES

Recent discoveries of oxygen-sensing mechanisms in different eukaryotic kingdoms allow us to compare molecular strategies dedicated to this task and the outputs that these produce. Remarkably, higher plants and animals converged, from a functional perspective, to recruit dioxygenase enzymes to posttranslationally modify transcriptional regulators for proteasomal degradation at the relatively “normoxic” conditions. In this way, transcriptional responses can be repressed at higher oxygen levels (which is context dependent) but are specifically elicited under hypoxia. The mitigation of the effects of prolonged hypoxia is also similar in animals and plants: reduction of metabolic rate, avoidance of toxicity of anaerobic by-products, and prevention of cell injury upon reoxygenation. Recent geological and phylogenetic investigations allow us to reconstruct the origin of such molecular switches in the eukaryotic clade and compare it with the development of organ-grade multicellularity. The results support the perspective that oxygen-consuming enzymes evolved sensory functions depending on the contingent requirements imposed by the environment and developmental programs. Considering that these sensing machineries evolved at a time (in the Neoproterozoic and early Paleozoic eras) when atmospheric oxygen concentrations were substantially lower than today, and in marine settings where redox is prone to vary, they may have played a major role in guiding development and homeostasis in response to endogenous oxygen dynamics. The broad scope of oxygen sensing and response machineries for multicellular success is further highlighted when hijacked during tumorigenesis to support uncontrolled growth in a variety of conditions and stresses.

OUTLOOK

The broad role of oxygen-sensing systems in the survival and evolution of complex multicellular life requires further exploration, including into the commonality and conservation of the oxygen-sensing machineries. That higher plants and animals adopted alternative solutions to direct their primary hypoxia responses, despite their ancestors likely being equipped with the same enzymatic repertoire, may describe differences in their respective environmental, cellular, and organismal features and histories. Broadly, by shifting focus from exploring oxygen-sensing mechanisms as primarily a response to oxygen shortage for aerobic respiration, we can potentially reveal previously unidentified ways in which these systems can be manipulated for clinical and agricultural benefit. By such an approach, we will gain further insight to their broad scope and the challenges that multicellular life is exposed to, today as in geologic history.

Eukaryotic kingdoms convergently recruited dioxygenases to sense fluctuations in ambient oxygen and to respond under hypoxia.

Oxygen sensing allows cells to attune their metabolism and fate to spatiotemporal requirements, a critical component in complex multicellularity. The basal oxygen-sensing mechanisms use alternative targets in plants, fungi, and animals—kingdoms that alone demonstrate the capacity to form tissues of different complexities.

Abstract

Oxygen-sensing mechanisms of eukaryotic multicellular organisms coordinate hypoxic cellular responses in a spatiotemporal manner. Although this capacity partly allows animals and plants to acutely adapt to oxygen deprivation, its functional and historical roots in hypoxia emphasize a broader evolutionary role. For multicellular life-forms that persist in settings with variable oxygen concentrations, the capacity to perceive and modulate responses in and between cells is pivotal. Animals and higher plants represent the most complex life-forms that ever diversified on Earth, and their oxygen-sensing mechanisms demonstrate convergent evolution from a functional perspective. Exploring oxygen-sensing mechanisms across eukaryotic kingdoms can inform us on biological innovations to harness ever-changing oxygen availability at the dawn of complex life and its utilization for their organismal development.

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Science

Too bright to breed

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Night light from coastal cities overpowers natural signals for coral spawning from neighboring reefs.

PHOTO: NOKURO/ALAMY STOCK PHOTO

Most coral species reproduce through broadcast spawning. For such a strategy to be successful, coordination has had to evolve such that gametes across clones are released simultaneously. Over millennia, lunar cycles have facilitated this coordination, but the recent development of bright artificial light has led to an overpowering of these natural signals. Ayalon et al. tested for the direct impact of different kinds of artificial light on different species of corals. The authors found that multiple lighting types, including cold and warm light-emitting diode (LED) lamps, led to loss of synchrony and spawning failure. Further, coastal maps of artificial lighting globally suggest that it threatens to interfere with coral reproduction worldwide and that the deployment of LED lights, the blue light of which penetrates deeper into the water column, is likely to make the situation even worse.

Curr. Biol. 10.1016/j.cub.2020.10.039 (2020).

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SpaceX launches Starlink app and provides pricing and service info to early beta testers

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SpaceX has debuted an official app for its Starlink satellite broadband internet service, for both iOS and Android devices. The Starlink app allows users to manage their connection – but to take part you’ll have to be part of the official beta program, and the initial public rollout of that is only just about to begin, according to emails SpaceX sent to potential beta testers this week.

The Starlink app provides guidance on how to install the Starlink receiver dish, as well as connection status (including signal quality), a device overview for seeing what’s connected to your network, and a speed test tool. It’s similar to other mobile apps for managing home wifi connections and routers. Meanwhile, the emails to potential testers that CNBC obtained detail what users can expect in terms of pricing, speeds and latency.

The initial Starlink public beta test is called the “Better than Nothing Beta Program,” SpaceX confirms in their app description, and will be rolled out across the U.S. and Canada before the end of the year – which matches up with earlier stated timelines. As per the name, SpaceX is hoping to set expectations for early customers, with speeds users can expect ranging from between 50Mb/s to 150Mb/s, and latency of 20ms to 40ms according to the customer emails, with some periods including no connectivity at all. Even with expectations set low, if those values prove accurate, it should be a big improvement for users in some hard-to-reach areas where service is currently costly, unreliable and operating at roughly dial-up equivalent speeds.

Image Credits: SpaceX

In terms of pricing, SpaceX says in the emails that the cost for participants in this beta program will be $99 per moth, plus a one-time cost of $499 initially to pay for the hardware, which includes the mounting kit and receiver dish, as well as a router with wifi networking capabilities.

The goal eventually is offer reliably, low-latency broadband that provides consistent connection by handing off connectivity between a large constellation of small satellites circling the globe in low Earth orbit. Already, SpaceX has nearly 1,000 of those launched, but it hopes to launch many thousands more before it reaches global coverage and offers general availability of its services.

SpaceX has already announced some initial commercial partnerships and pilot programs for Starlink, too, including a team-up with Microsoft to connect that company’s mobile Azure data centers, and a project with an East Texas school board to connect the local community.

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Erratum for the Report “Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances” by R. Van Klink, D. E. Bowler, K. B. Gongalsky, A. B. Swengel, A. Gentile, J. M. Chase

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S. Rennie, J. Adamson, R. Anderson, C. Andrews, J. Bater, N. Bayfield, K. Beaton, D. Beaumont, S. Benham, V. Bowmaker, C. Britt, R. Brooker, D. Brooks, J. Brunt, G. Common, R. Cooper, S. Corbett, N. Critchley, P. Dennis, J. Dick, B. Dodd, N. Dodd, N. Donovan, J. Easter, M. Flexen, A. Gardiner, D. Hamilton, P. Hargreaves, M. Hatton-Ellis, M. Howe, J. Kahl, M. Lane, S. Langan, D. Lloyd, B. McCarney, Y. McElarney, C. McKenna, S. McMillan, F. Milne, L. Milne, M. Morecroft, M. Murphy, A. Nelson, H. Nicholson, D. Pallett, D. Parry, I. Pearce, G. Pozsgai, A. Riley, R. Rose, S. Schafer, T. Scott, L. Sherrin, C. Shortall, R. Smith, P. Smith, R. Tait, C. Taylor, M. Taylor, M. Thurlow, A. Turner, K. Tyson, H. Watson, M. Whittaker, I. Woiwod, C. Wood, UK Environmental Change Network (ECN) Moth Data: 1992-2015, NERC Environmental Information Data Centre (2018); .

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