Ultraviolet radiation (UV) is a crucial abiotic stressor that can have severe impacts on biota residing in the upper euphotic zone, especially if UV stress coincides with other stressors such as ...extreme sea surface temperatures (SSTs). Exposure-dependent effects of UV exposure have been described for a broad range of marine taxa and ecosystems such as coral reefs, yet little is known about the magnitude and seasonality of UV exposure in natural waters. In the present study, we determined how daily exposure of UV-B and UV-A varies seasonally along the water column of a reef system in the central Red Sea, and identified periods when damaging UV levels are likely to coincide with episodes of extreme SST, both presently and in the future. Between July 2016 and September 2018, UV spectroradiometer profiles were recorded fortnightly at a pelagic site adjacent to a mid-shore reef off the Saudi Arabian Red Sea coast, while atmospheric UV-B and UV-A irradiances were measured in 10-minute intervals. Additionally, we quantified the concentration of chlorophyll-a (Chl-a) and absorption by chromophoric dissolved organic matter (aCDOM) in the reef as well as the surrounding waters. Biologically effective optical depths (Z10%) ranged from 6.3–12.9 m (UV-B) and 14.4–27.3 m (UV-A), with the highest UV transparency being observed in late summer when photodegradation of dissolved organic matter (DOM) was most intense and the concentration and molecular weight of CDOM were at their lowest. Incident UV peaked a few weeks prior to this later summer maximum in UV transparency. Consequently, organisms living close to the water surface experienced their most intense UV exposure in May/June, while the timing of maximum UV exposure for biota below ~ 2–4 m coincided with the annual peak in water transparency and water temperature, i.e., in July/August. However, SSTs in the Red Sea are increasing at a rapid rate due to climate change, with the consequence that extreme temperatures are occurring earlier in the year and may eventually coincide with extreme UV radiation in shallower areas of the reef. This development could have potentially detrimental effects on highly sensitive, immotile reef biota such as reef-building corals.
Despite being exposed to extreme water temperatures and solar irradiances, Red Sea corals are relatively resistant to bleaching. While their thermal tolerance is well described, little is known about ...their resistance to ultraviolet-B radiation (UVB). Here, we performed a short-term (2 days) UVB-removal incubation with
Stylophora pistillata
, and
in situ
measurements with
Pocillopora verrucosa
complemented by a long-term (46 days) transplantation and UVB-removal experiment. Using a suite of physiological parameters (effective quantum yield (
F
v
’/
F
m
’), oxidative stress (lipid peroxidation, LPO), and primary production), we assessed the impacts of UVB on the physiology and acclimation capacity of Red Sea corals. Shielding
S. pistillata
from UVB did not change the gross primary production or
F
v
’/
F
m
’, and respiration and LPO in the host remained unaffected. In situ,
P. verrucosa
exhibited less varying and significantly higher
F
v
’/
F
m
’ in 8 m depth (0.61 ± 0.04) than in 4 m (0.52 ± 0.06), 2 m (0.51 ± 0.09), and 0.5 m (0.50 ± 0.11), where water temperatures ranged from 30.5–33.4, 30.6–34.0, 30.8–34.5, 30.6–37.3°C and daily UVB exposures averaged 0.9, 2.9, 11.8 and 21.4 kJ m
-2
, respectively.
F
v
’/
F
m
’ correlated the strongest with UVB (-0.57), followed by PAR (-0.54) and temperature (-0.40), suggesting that UVB is a key determinant of photosynthetic efficiency.
F
v
’/
F
m
’ of upward transplanted specimens (T 1m) was initially decreased but gradually increased and reached the same values as shallow corals (1 m) after 44 days. UVB removal significantly increased the
F
v
’/
F
m
’ of transplanted corals in the first 20 days. Oxidative stress was initially highest in T 1m samples under full sunlight but equalized with 1 m specimens by day 46, whereas oxidative stress was significantly reduced by day 4 in T 1m corals sheltered from UVB. Overall, UVB-removal generally had little impact on the physiology of shallow-water
S. pistillata
and
P. verrucosa
but considerably accelerated the acclimation of upward transplanted corals. Our study highlights that UVB is a crucial stressor governing the photoacclimation capacity of these Red Sea coral species.
has emerged as a powerful green cell factory for metabolic engineering of sustainable products created from the photosynthetic lifestyle of this microalga. Advances in nuclear genome modification and ...transgene expression are allowing robust engineering strategies to be demonstrated in this host. However, commonly used lab strains are not equipped with features to enable their broader implementation in non-sterile conditions and high-cell density concepts. Here, we used combinatorial chloroplast and nuclear genome engineering to augment the metabolism of the
strain UVM4 with publicly available genetic tools to enable the use of inorganic phosphite and nitrate as sole sources of phosphorous and nitrogen, respectively. We present recipes to create phosphite-buffered media solutions that enable high cell density algal cultivation. We then combined previously reported engineering strategies to produce the heterologous sesquiterpenoid patchoulol to high titers from our engineered green cell factories and show these products are possible to produce in non-sterile conditions. Our work presents a straightforward means to generate
strains for broader application in bio-processes for the sustainable generation of products from green microalgae.
The photosymbiosis of tropical giant clams (subfamily Tridacninae) with unicellular algae (Symbiodiniaceae) restricts their distribution to the sunlit, shallow waters of the euphotic zone where ...organisms are additionally exposed to potentially damaging levels of solar UV radiation. Metabolic and physiological responses of Red Sea
Tridacna maxima
clams, including net calcification and primary production, as well as valvometry (i.e., shell gaping behavior) were assessed when exposed to simulated high radiation levels received at 3 and 5 m underwater. The two levels of radiation included exposure treatments to photosynthetically active radiation (PAR; 400–700 nm) alone and to both, PAR and ultraviolet-B radiation (UV-B; 280–315 nm). The valvometry data obtained using flexible magnetic sensors indicated that specimens under PAR + UV-B exposure significantly reduced the proportion of their exposed mantle area, a potential photo-protective mechanism which, however, reduces the overall amount of PAR received by the algal symbionts. Consequently, specimens under PAR + UV-B displayed a slight, although non-significant, reduction in primary production rates but no signs of additional oxidative stress, changes in symbiont densities, chlorophyll content, or levels of mycosporine-like amino acids. Net calcification rates of
T. maxima
were not affected by exposure to UV-B; however, calcification was positively correlated with incident PAR levels. UV-B exposure changes the valvometry, reducing the exposed mantle area which consequently diminishes the available PAR for the photosymbionts. Still,
T. maxima
maintains high rates of primary production and net calcification, even under high levels of UV-B. This provides experimental support for a recently described, effective UV-defensive mechanism in Tridacninae, in which the photonic cooperation of the associated algal symbionts and giant clam iridocytes is assumed to establish optimal conditions for the photosynthetic performance of the clams’ symbionts.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OBVAL, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Isoprene is a clear, colorless, volatile 5-carbon hydrocarbon that is one monomer of all cellular isoprenoids and a platform chemical with multiple applications in industry. Many plants have evolved ...isoprene synthases (IspSs) with the capacity to liberate isoprene from dimethylallyl diphosphate (DMADP) as part of cellular thermotolerance mechanisms. Isoprene is hydrophobic and volatile, rapidly leaves plant tissues and is one of the main carbon emission sources from vegetation globally. The universality of isoprenoid metabolism allows volatile isoprene production from microbes expressing heterologous IspSs. Here, we compared heterologous overexpression from the nuclear genome and localization into the plastid of four plant terpene synthases (TPs) in the green microalga Chlamydomonas reinhardtii. Using sealed vial mixotrophic cultivation, direct quantification of isoprene production was achieved from the headspace of living cultures, with the highest isoprene production observed in algae expressing the Ipomoea batatas IspS. Perturbations of the downstream carotenoid pathway through keto carotenoid biosynthesis enhanced isoprene titers, which could be further enhanced by increasing flux towards DMADP through heterologous co-expression of a yeast isopentenyl-DP delta isomerase. Multiplexed controlled-environment testing revealed that cultivation temperature, rather than illumination intensity, was the main factor affecting isoprene yield from the engineered alga. This is the first report of heterologous isoprene production from a eukaryotic alga and sets a foundation for further exploration of carbon conversion to this commodity chemical.
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•Ipomoea batatas isoprene synthase was the most active in alga.•Isoprene production was enhanced in ketocarotenoid producing transformants.•Isoprene production was enhanced by isomerase co-expression.•Temperature, rather than illumination, most affected isoprene titers.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Ocean acidification (OA) may interact with anthropogenic pollutants, such as heavy metals (HM), to represent a threat to marine organisms and ecosystems. Here, we perform a quantitative meta-analysis ...to examine the combined effects of OA and heavy metals on marine organisms. The results reveal predominantly additive interactions (67%), with a considerable proportion of synergistic interactions (25%) and a few antagonistic interactions (8%). The overall adverse effects of heavy metals on marine organisms were alleviated by OA, leading to a neutral impact of heavy metals in combination with OA. However, different taxonomic groups showed large variabilities in their responses, with microalgae being the most sensitive when exposed to heavy metals and OA, and having the highest proportion of antagonistic interactions. Furthermore, the variations in interaction type frequencies are related to climate regions and heavy metal properties, with antagonistic interactions accounting for the highest proportion in temperate regions (28%) and when exposed to Zn (52%). Our study provides a comprehensive insight into the interactive effects of OA and HM on marine organisms, and highlights the importance of further investigating the responses of different marine taxonomic groups from various geographic locations to the combined stress of OA and HM.
Ocean acidification is recognized as a major anthropogenic perturbation of the modern ocean. While extensive studies have been carried out to explore the short-term physiological responses of ...phytoplankton to ocean acidification, little is known about their lipidomic responses after a long-term ocean acidification adaptation. Here we perform the lipidomic analysis of a marine diatom
Phaeodactylum tricornutum
following long-term (∼400 days) selection to ocean acidification conditions. We identified a total of 476 lipid metabolites in long-term high CO
2
(i.e., ocean acidification condition) and low CO
2
(i.e., ambient condition) selected
P. tricornutum
cells. Our results further show that long-term high CO
2
selection triggered substantial changes in lipid metabolites by down- and up-regulating 33 and 42 lipid metabolites. While monogalactosyldiacylglycerol (MGDG) was significantly down-regulated in the long-term high CO
2
selected conditions, the majority (∼80%) of phosphatidylglycerol (PG) was up-regulated. The tightly coupled regulations (positively or negatively correlated) of significantly regulated lipid metabolites suggest that the lipid remodeling is an organismal adaptation strategy of marine diatoms to ongoing ocean acidification. Since the composition and content of lipids are crucial for marine food quality, and these changes can be transferred to high trophic levels, our results highlight the importance of determining the long-term adaptation of lipids in marine producers in predicting the ecological consequences of climate change.
The tropical and subtropical oceans experience intense incident ultraviolet radiation (280–400 nm) while their water columns are thought to be highly transparent. This combination represents a high ...potential for harmful effects on organisms, yet only few reports on the UV penetration properties of oligotrophic tropical waters exist. Here, we present the pattern of UV attenuation over a wide latitudinal range of the oligotrophic Red Sea. We recorded spectroradiometer profiles of PAR and UV, together with chlorophyll‐a (Chl‐a) and light absorption by chromophoric dissolved organic matter (CDOM) to determine the contribution of phytoplankton and CDOM toward UV attenuation. Transparency to UV exhibited a distinct latitudinal gradient, with the lowest and highest diffuse attenuation coefficients at 313 nm (Kd (313)) of 0.130 m−1 and 0.357 m−1 observed at the northern coast off Duba, and in the south close to the Farasan islands, respectively. Phytoplankton and CDOM both modulated UV attenuation, but CDOM was found to be the key driver despite the lack of riverine inputs. We confirm that ultraviolet radiation can reach deeper into the Red Sea than previously described, which means its potential to act as a stressor and selective driver for Red Sea organisms may have been underestimated to date.
The optical properties of the oligotrophic and highly transparent Red Sea represented by the downwelling diffuse attenuation coefficients (Kd) for the integrated PAR (400–700 nm), UV‐A (320–400 nm) and UV‐B spectra (280–320 nm). PAR and UV‐B were measured during four Red Sea cruises between October 2016 and March 2018, while the UV‐A properties were determined as part of two cruises in August 2017 and March 2018.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Microbial production of heterologous metabolites is now a mature technology in many host organisms, opening new avenues for green production processes of specialty chemicals. At lab scale, ...petroleum-based hydrophobic bio-compatible solvents like dodecane can be used as a second phase on top of microbial cultures to act as a physical sink for heterologous hydrocarbon products like isoprenoids. However, this approach has significant drawbacks at scale due to the difficulty of handling solvents and their potential contamination with unwanted byproducts of their manufacture. We discovered that synthetic perfluorocarbon liquids (FCs), commonly used for heat transfer, can also act as physical sinks for microbially produced isoprenoid compounds. FCs are stable, inert, and are amenable to direct liquid–liquid extraction with alcohols for rapid product isolation. These liquids are more dense than water and form a lower phase to microbial cultures rather than an upper phase as with other solvents. Their ability to form an under-layer or ‘underlay’ also enables the cultivation of microbes directly at the FC–culture medium interface
via
gravity settling, which could open their application for filamentous or mat-forming organisms. We present comparisons of the isoprenoid extraction potential of three commercial FCs: FC-3283, FC-40, and FC-770 with engineered green microalga cultures producing patchoulol, taxadiene, casbene, or 13
R
(+) manoyl oxide. We demonstrate that FCs are promising alternatives to traditional solvents and open new avenues in bio-process design for microbial heterologous metabolite milking.
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IJS, KILJ, NUK, UL, UM, UPUK
Microbial production of heterologous metabolites is now a mature technology in many host organisms, opening new avenues for green production processes of specialty chemicals. At lab scale, ...petroleum-based hydrophobic bio-compatible solvents like dodecane can be used as a second phase on top of microbial cultures to act as a physical sink for heterologous hydrocarbon products like isoprenoids. However, this approach has significant drawbacks at scale due to the difficulty of handling solvents and their potential contamination with unwanted byproducts of their manufacture. We discovered that synthetic perfluorocarbon liquids (FCs), commonly used for heat transfer, can also act as physical sinks for microbially produced isoprenoid compounds. FCs are stable, inert, and are amenable to direct liquid-liquid extraction with alcohols for rapid product isolation. These liquids are more dense than water and form a lower phase to microbial cultures rather than an upper phase as with other solvents. Their ability to form an under-layer or 'underlay' also enables the cultivation of microbes directly at the FC-culture medium interface
via
gravity settling, which could open their application for filamentous or mat-forming organisms. We present comparisons of the isoprenoid extraction potential of three commercial FCs: FC-3283, FC-40, and FC-770 with engineered green microalga cultures producing patchoulol, taxadiene, casbene, or 13
R
(+) manoyl oxide. We demonstrate that FCs are promising alternatives to traditional solvents and open new avenues in bio-process design for microbial heterologous metabolite milking.
A novel bioprocess to capture and purify terpenoids produced by engineered microbes using 2-phase cultivation of the algae with liquid perfluorocarbons followed by liquid-liquid extraction of the terpenoids with ethanol.
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IJS, KILJ, NUK, UL, UM, UPUK
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