Exposure of marine life to low oxygen is accelerating worldwide via climate change and localized pollution. Mass coral bleaching and mortality have recently occurred where reefs have experienced chronic low oxygen events. However, the mechanistic basis of tolerance to oxygen levels inadequate to sustain normal functioning (i.e. hypoxia) and whether it contributes to bleaching susceptibility, remain unknown. We therefore experimentally exposed colonies of the environmentally resilient Acropora tenuis, a common reef‐building coral from the Great Barrier Reef, to deoxygenation–reoxygenation stress that was aligned to their natural night–day light cycle. Specifically, the treatment involved removing the ‘night‐time O2 buffer’ to challenge the inherent hypoxia thresholds. RNA‐Seq analysis revealed that coral possess a complete and active hypoxia‐inducible factor (HIF)‐mediated hypoxia response system (HRS) homologous to other metazoans. As expected, A. tenuis exhibited bleaching resistance and showed a strong inducibility of HIF target genes in response to deoxygenation stress. We applied this same approach in parallel to a colony of Acropora selago, known to be environmnetally susceptible, which conversely exhibited a bleaching phenotype response. This phenotypic divergence of A. selago was accompanied by contrasting gene expression profiles indicative of varied effectiveness of their HIF‐HRS. Based on our RNA‐Seq analysis, we propose (a) that the HIF‐HRS is central for corals to manage deoxygenation stress and (b) that key genes of this system (and the wider gene network) may contribute to variation in coral bleaching susceptibility. Our analysis suggests that heat shock protein (hsp) 70 and 90 are important for low oxygen stress tolerance and further highlights how hsp90 expression might also affect the inducibility of coral HIF‐HRS in overcoming a metabolic crisis under deoxygenation stress. We propose that differences in coral HIF‐HRS could be central in regulating sensitivity to other climate change stressors—notably thermal stress—that commonly drive bleaching.
24 September 2018 in Environmental Science & Technology
Assessing patterns of phytoplankton primary productivity over space and time has remained a key goal for oceanographers and limnologists for over two centuries. The introduction of active chlorophyll-a based fluorometers several decades ago provided a potential means to realise this goal with unprecedented spatio-temporal resolution and scale. Yet, despite notable uptake of one particular technique, Fast Repetition Rate fluorometry (FRRf) in the past 20 years, this technology has arguably failed to live up to its early promise of becoming the “go-to” tool for measuring aquatic primary production (PP). Undoubtedly, the major obstacle to wider implementation of FRRf in PP studies has been the conversion of FRRf measurements of photosynthesis, in rates of electron transfer (ETR), to equivalent rates of CO2-uptake that carry most relevance in biogeochemical studies. Uncertainty surrounding this conversion stems partly from methodological inconsistencies between studies, but perhaps more fundamentally from our limited understanding of how the “electron requirement for carbon fixation” (KC or e,C) is influenced by both the environment, and by differences in the composition and physiology of phytoplankton assemblages. Within this critical review, we therefore propose a forward-thinking “roadmap” for minimising methodological bias associated with measurements of e,C, while simultaneously developing a better mechanistic understanding of the ecophysiology underlying the conversion of electrons to fixed carbon. To do this, we re-evaluate core physiological processes governing how microalgae invest photosynthetic electron transport-derived energy and reductant into cellular-retained carbon versus alternative sinks. We then use this information to propose a series of steps to facilitate the broader uptake and exploitation of FRRf and of FRRf-variant approaches, which could transform our knowledge of aquatic PP. In so doing, we argue that it may be time to revise our historic methodological focus on carbon as the currency of aquatic primary productivity, to better appreciate that electron transport fundamentally drives ecosystem biogeochemistry, modulates cell-to-cell interactions, and ultimately modifies community biomass and structure.
Summary: Symbiodiniaceae are a diverse family of marine dinoflagellates, well known as coral endosymbionts. Isolation and in vitro culture of Symbiodiniaceae strains for physiological studies is a widely adopted tool, especially in the context of understanding how environmental stress perturbs Symbiodiniaceae cell functioning. While the bacterial microbiomes of corals often correlate with coral health, the bacterial communities co‐cultured with Symbiodiniaceae isolates have been largely overlooked, despite the potential of bacteria to significantly influence the emergent physiological properties of Symbiodiniaceae cultures. We examined the physiological response to heat stress by Symbiodiniaceae isolates (spanning three genera) with well‐described thermal tolerances, and combined these observations with matched changes in bacterial composition and abundance through 16S rRNA metabarcoding. Under thermal stress, there were Symbiodiniaceae strain‐specific changes in maximum quantum yield of photosystem II (proxy for health) and growth rates that were accompanied by changes in the relative abundance of multiple Symbiodiniaceae‐specific bacteria. However, there were no Symbiodiniaceae‐independent signatures of bacterial community reorganisation under heat stress. Notably, the thermally tolerant Durusdinium trenchii (ITS2 major profile D1a) had the most stable bacterial community under heat stress. Ultimately, this study highlights the complexity of Symbiodiniaceae‐bacteria interactions and provides a first step towards uncoupling their relative contributions towards Symbiodiniaceae physiological functioning.
Nitrogen (N) availability affects phytoplankton photosynthetic performance and regulates marine primary production (MPP) across the global coast and oceans. Bio‐optical tools including Fast Repetition Rate fluorometry (FRRf) are particularly well suited to examine MPP variability in coastal regions subjected to dynamic spatio‐temporal fluctuations in nutrient availability. FRRf determines photosynthesis as an electron transport rate through Photosystem II (ETRPSII), requiring knowledge of an additional parameter, the electron requirement for carbon fixation (KC), to retrieve rates of CO2‐fixation. KC strongly depends upon environmental conditions regulating photosynthesis, yet the importance of N‐availability to this parameter has not been examined. Here, we use nutrient bioassays to isolate how N (relative to other macronutrients P, Si) regulates KC of phytoplankton communities from the Australian coast during summer, when N‐availability is often highly variable. KC consistently responded to N‐amendment, exhibiting up to a threefold reduction and hence an apparent increase in the efficiency with which electrons were used to drive C‐fixation. However, the process driving this consistent reduction was dependent upon initial conditions. When diatoms dominated assemblages and N was undetectable (e.g., post bloom), KC decreased predominantly via a physiological adjustment of the existing community to N‐amendment. Conversely, for mixed assemblages, N‐addition achieved a similar reduction in KC through a change in community structure toward diatom domination. We generate new understanding and parameterization of KC that is particularly critical to advance how FRRf can be applied to examine C‐uptake throughout the global ocean where nitrogen availability is highly variable and thus frequently limits primary productivity.