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Aquatic plants: Life support and nutrition in space: Comparison
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Please note this is a comparison between Version 2 by Lindsay Dong and Version 1 by Stephanie Polutchko.

Sustainable long-term space missions require regenerative life support from plants. However, traditional crop plants lack some features desirable for use in space environments. The aquatic plant family Lemnaceae (duckweeds) has enormous potential as a space crop, featuring (i) fast growth, with very high rates of O2 production and CO2 sequestration, (ii) an exceptional nutritional quality (with respect to radiation-fighting antioxidants and high-quality protein), (iii) easy propagation and high productivity in small spaces, and (iv) resilience to the stresses (radiation, microgravity, and elevated CO2) of the human-inhabited space-cabin environment. These attractive traits of Lemnaceae are placed into the context of their unique adaptations to the aquatic environment. In other words, evolution may have led to a group of plants with traits that can be viewed as pre-adaptations for spaceflight environments.

  • duckweed
  • homeostasis
  • Lemnaceae
  • reactive oxygen species

1. Introduction

1.1. Molecular Oxygen Plays Unique and Essential Roles for Life

Molecular oxygen (O2) is necessary for much of life on Earth to function. Most of the oxygen in the atmosphere has been produced over the last two billion years by photosynthetic organisms, which supported the evolution of multicellular organisms that depend on aerobic respiration [1][2]. This dependency applies to both heterotrophs and autotrophs, such as plants that can be killed when roots have diminished access to oxygen because of insufficient O2-dependent respiration in water-logged soils [3] (except for specialist plants with unique adaptations facilitating O2 diffusion to the roots[4]).

For space travel and habitation, enough O2 must be transported or continuously generated for long missions to sustain a human crew. Currently, O2 is produced on the International Space Station through the splitting of water by electrolysis [5]. For long human-crewed space missions, plants can serve as a regenerative life support system that continuously produces O2, removes CO2 [6][7], and provides additional essential services.

1.2. Reactive Oxygen Can Kill

While essential for much of life on earth, oxygen is a double-edged sword. The first mass extinction event of biological species was likely caused by the rise in atmospheric O2 levels and has been termed the Great Oxidation Event[8][9]. Today, O2-dependent organisms carefully maintain an internal balance between oxidants and antioxidants (redox homeostasis) [10]. Notably, energy metabolism in chloroplasts and mitochondria (the organellar powerhouses that interact with O2) continuously creates a particularly reactive form of oxygen (reactive oxygen, species, ROS; [10][11]). Whereas ROS are essential in small doses, excess ROS can cause a host of adverse effects (see below). The life-supporting quality of oxygen is thus inextricably linked to its potential dangers.

In small quantities, ROS act as universal regulators of master control genes that orchestrate growth, development, aging, and various metabolic defenses of humans, plants, and many microorganisms [12][13]. For example, ROS can stimulate cell division (by forwarding the cell cycle) as well as trigger the destruction of (typically unwanted or injured) cells in the process of programmed cell death [14][15], both of which can be enhanced to undesirable levels in spaceflight environments [16] (for details, see the next section). One example of an ROS is superoxide (a form of O2 with a single additional electron, i.e, superoxide anion radical, O2●−), which various organisms actively produce to kill pathogens [17] and other unwanted cells. However, excess superoxide can cause excessive cell damage unless redox homeostasis is maintained by keeping ROS in check with antioxidants. A lasting departure from redox homeostasis can cause continuous low-grade activation of the human immune system with system-wide inflammation and a host of resulting diseases, disorders, and dysfunctions. In large quantities, ROS can be lethal. In viral diseases (such as HIV-AIDS and, evidently, COVID-19), snowballing production of ROS and other inflammation-promoting messengers (the cytokine storm) can lead to massive organ damage [18].

2. The Challenges of Space Environments

A major challenge for human utilization of space is exposure to galactic cosmic radiation (GCR). GCR consists of heavy ions/high-density charged particles [16][19] and can generate dangerous amounts of ROS through the splitting of water under the influence of radiation (radiolysis) in all water-containing cells. This ROS can lead to DNA mutations. In addition, GCR can also produce direct DNA breaks (Figure 1; [20]). The effects of GCR-induced ROS on gene regulation are complex and include induction of some protective (e.g., antioxidant) effects as well as negative snowballing effects that further exacerbate ROS production and DNA damage. For example, a feed-forward cycle in space environments involves ROS stimulation of a human ROS-producing enzyme (NADPH oxidase; [21][22]). Specifically, an initial wave of ROS production triggers consecutive waves of ROS production to activate and recruit other immune cells (as may be warranted under pathogen attack [15]). Excess ROS production and DNA damage can thus lead to signaling cascades that produce more and more unwanted ROS (Figure 1).

/media/item_content/202206/62abd0ee4ed35oxygen-02-00016-g001.png
Figure 1. A schematic flowchart of how galactic cosmic radiation can lead to the production of ROS and DNA damage. Both ROS and DNA damage can either encourage (pink arrows) or prevent (pink T-shaped lines) multiple gene regulation events, including those that support (blue arrow) or prevent (pink T-shaped line) DNA repair.

3. The Multi-Hit Hypothesis: Interaction among Different Stresses in a Space Environment

3.1. Specific Plant Responses

In land plants, a low level of gravity (microgravity) can interfere with plant responses to radiation by inhibiting directional, gravity-dependent signals between shoots and roots [23]. More research is needed into the effect of microgravity in space environments as different species can respond in different ways [24].

Elevated CO2 in a confined environment is also a concern. Plants growing under elevated atmospheric CO2 levels can produce excessive levels of ROS (Figure 2), which can lead to an imbalance in redox homeostasis [25]. Specifically, elevated CO2 can enhance ROS production when photosynthesis utilizes the greater level of available CO2 to produce more sugars and starch. This results in a build-up of carbohydrates and a backup of electrons in the photosynthetic electron transport chain. In turn, this backup leads to the transfer of electrons and/or excitation energy to oxygen, forming ROS [25]. Most plants respond to prolonged exposure to elevated CO2 with photosynthetic downregulation because the plant can perform the same rate of photosynthesis (as under lower CO2 levels) with fewer photosynthetic proteins under elevated CO2. CO2 has also been reported to accelerate plant aging (senescence; Figure 2; [26]). In some species, growth can be inhibited by elevated CO2 alone [27], and it is common for elevated CO2 to exacerbate growth penalties imposed by other environmental factors [28][29][30][31].

/media/item_content/202206/62abd102cb119oxygen-02-00016-g002.png
Figure 2. Flowchart depicting the causes (top boxes) and effects (bottom boxes) of reactive oxygen species (middle box) in plants (green; left) and humans (red; right).

3.2. Human Physiology

To mitigate the risks associated with spaceflight, it is important to consider multiple lifestyle factors for humans [32]. Diet, physical activity, and psychological stress (Figure 2) all provide inputs into cellular redox homeostasis and thus affect health outcomes [33][34]. For example, whereas regular moderate physical activity triggers the synthesis of endogenous antioxidant enzymes to combat ROS production during exercise, physical inactivity fails to induce antioxidant enzymes [35] and thus fails to counter ROS production (Figure 2). It thus appears that these other factors, which are modifiable to some extent, may either exacerbate or mitigate human exposure to GCR in spaceflight environments.

4. Redox-Based Orchestration of Growth, Development, and Defenses

4.1. Early-Warning Systems for Oxidative Stress

A hallmark of metabolically active cells is that they allow moderate amounts of ROS to play fundamental roles in cellular metabolism and other biological processes [36][37] while avoiding unwanted effects of excess ROS. To support this redox homeostasis, large molecules, including fatty acids-based lipids and proteins, are particularly sensitive to oxidation. These molecules can serve as sentinels, and signal when internal ROS production is rising. For example, membranes surrounding cells contain polyunsaturated fatty acids (PUFAs) derived from dietary fats; these membrane components are easily oxidized to oxidation products that serve as gene regulators [38][39]. In humans, immunostimulatory regulators are mainly derived from omega-6 PUFAs and inflammation-resolving regulators mainly from omega-3 PUFAs [40]. In addition, proteins with (thiol) groups that are easily oxidized are also linked to redox-based gene-regulation [41][42][43].

4.2. Gene Regulation by Derivatives of Lipid Peroxidation and the Need for Dietary Antioxidant Metabolites

Just like ROS and their products, antioxidant systems are potent modulators of redox-modulated signaling networks and genes[44]. Dietary membrane-embedded antioxidants keep the formation of PUFA-derived regulators in check and thus control and resolve acute inflammation in humans[45]. Furthermore, a balanced dietary ratio of omega-3 to omega-6 fatty acids is critical to support immunity and avoid non-resolving inflammation.

The human brain is particularly susceptible to non-resolving inflammation due to its large complement of biological membranes, and a high level of oxygenation that increases the propensity for PUFA oxidation[46][47][48]. Resulting non-resolving neuroinflammation leads to low cognitive function in otherwise healthy individuals as well as to mental and learning disorders and neurodegenerative diseases[34][49]. Antioxidation is therefore needed to prevent neuroinflammation[34][50].

Whereas a whole suite of diet-derived antioxidant metabolites can provide protection in aqueous (water-based) environments, only a few antioxidants are able to dissolve and provide protection in biological membranes. These latter membrane-soluble (fat-soluble) antioxidants include the antioxidant vitamin E (tocopherol) and carotenoids[34][51][52]. The structure of these molecules determines their orientation in the membrane, and two carotenoids in particular (zeaxanthin and lutein) integrate into biological membranes in a way that can provide stabilization[53] and oppose PUFA oxidation[34][54][55][56]. Zeaxanthin is the more potent antioxidant of the two[57], exhibiting a particularly stabilizing orientation in biological membranes[58].

4.3. Zeaxanthin and Lutein Protect Photosynthesis

Unlike humans, plants can make zeaxanthin and lutein from scratch (de novo) for specific roles in the prevention of radiation damage. However, whereas lutein is constitutively present in leafy crops, zeaxanthin is formed only under bright light and quickly removed again when light levels drop in these photosynthetic systems[59]. Only leafy greens harvested and eaten immediately after their exposure to bright light thus deliver significant levels of zeaxanthin. In contrast, leafy green produce purchased at a grocery store provides lutein but little to no zeaxanthin. Moreover, typical edible leafy crops accumulate much less zeaxanthin than the inedible leaves of evergreens[59]. Still, foods other than leaves can provide high levels of zeaxanthin and lutein on earth, including orange peppers, corn, and eggs (Figure 3;[60][61][62][63]). Zeaxanthin was named after the yellow color of an ear of corn (genus Zea, with “xanthos” the Greek word for golden/yellow). While being unable to synthesize carotenoids de novo, most animals do accumulate carotenoids when they have access to carotenoid-containing food[64]. The problem in spaceflight environments, however, is that there won’t be room for a corn field or a chicken farm and that typical edible crops produce very little zeaxanthin when evidence points to a need for human consumption of both zeaxanthin and lutein. As illustrated below (see section 5), aquatic floating plants have the unusual property of accumulating as much and more zeaxanthin as the inedible leaves of evergreen plants.

/media/item_content/202206/62abd1cb0d15coxygen-02-00016-g003.png
Figure 3. Images of whole food sources that contain high levels of zeaxanthin and lutein including, duckweed (see below), eggs (see above), orange peppers (see above), and corn (see above).

In addition, zeaxanthin does not act alone in providing the necessary protection for humans. To extend the lifetime of zeaxanthin and vitamin E in membranes, they must be recycled (by other antioxidants donating an electron and re-reducing oxidized zeaxanthin or vitamin E) to prevent them from becoming harmful oxidants themselves (Figure 4; [65][66]). It is thus critical to provide a balanced mix of antioxidant metabolites in the human diet, preferably through the consumption of whole foods rich in multiple essential micronutrients [67]. In contrast, single, high-dose antioxidant supplementation can have negative effects[68]. Specifically, excess dietary consumption of antioxidants from high-dose supplements can lower ROS levels to the extent that essential ROS signals fail to be produced[35]. Due to the benefits of whole food as well as the finite lifetime of vitamin supplements, nutritious crops will be critical to extended space missions.

/media/item_content/202206/62abd1e38c3dfoxygen-02-00016-g004.png
Figure 4. A schematic depiction of the interconnectedness of duckweed (left) and astronauts (right). In the center is a schematic depiction of the intertwined cycle of detoxification of ROS and the recycling of vitamin E and zeaxanthin by water-soluble antioxidants. A mother frond (leaf-like structure) is the initial source for photosynthetically produced sugars and its daughter fronds and rootlets are sinks for the sugars until the synthesis of sugars by daughter fronds exceeds the import of sugars and they, in turn, become source tissues.

5. Lemnaceae as Space Crops

5.1. An Unusual Combination of Multiple Attractive Traits

The enormous potential of the aquatic plant family Lemnaceae (duckweeds) as both model species (for, e.g., radiobiology and genomic studies) and edible space crops has been recognized since the beginning of the space program (Figure 5). Lemnaceae were the very first plants studied for photosynthesis in space, grew well under these conditions[69], and have been recommended as a good candidate for bioregenerative life support systems[70][71][72][73]. Additional flight experiments, including NASA STS-4 Getaway Special (1982), Russian satellite Bion 8 (1987), Russian satellite Bion 10 (1992), NASA STS-60 Getaway Special (1994), and STS-67 (1995), indicated that Lemnaceae are also tolerant of the GCR and microgravity encountered in space.

/media/item_content/202206/62abd1fed32ceoxygen-02-00016-g005.png
Figure 5. Summary of Lemnaceae features suitable for spaceflight environments (light orange text boxes) and brief explanations (white text boxes) below each point. See text for additional details.

Lemnaceae are consumed around the globe and hailed as a new superfood (e.g.,[74]), and also possess multiple features that make them particularly attractive candidates for space crops (Figure 5). In addition to fast growth, which entails very high rates of O2 production and CO2 removal, Lemnaceae have an exceptional nutritional quality (especially radiation-fighting antioxidants and high-quality protein with all essential amino acids for humans); they are also highly volume-efficient (with particularly small size and the complete or near-complete absence of non-photosynthetic parts) and easy to grow[75].

5.2. Can the Aquatic Lifestyle Be Seen as a Pre-Adaptation for Spaceflight Environments

The attractive traits of Lemnaceae for spaceflight environments summarized in Figure 5 can be traced back to apparent selective pressures acting on plants in aquatic environments[31]. To design a plant suitable as a regenerative life support system for a space environment (Figure 4), one would want the plant to consist mainly, or only, of leaves—that produce O2 and take in CO2—with little to no tissue allocated to stems, roots, or any other parts that consume O2 and release CO2. Aquatic plants like the Lemnaceae naturally consist mostly or entirely of photosynthetic tissue. Duckweed’s total or almost total absence of non-photosynthetic tissue makes it such that all photosynthetically produced sugar can be reinvested in more photosynthetic tissue that supports more O2 production and sequesters more CO2. By re-investing most, or all, photosynthetically produced sugars into additional photosynthetic tissue, aquatic plants can also sustain much higher growth rates than land plants that must invest substantial resources in non-photosynthetic tissues (see Figure 5; [76])

5.3. Exceptional Antioxidant Content

Duckweeds are an exception to the general trend that fast-growing edible crops do not accumulate large amounts of zeaxanthin in their leaves. Two species of duckweed showed similarly high levels of zeaxanthin accumulation as the inedible leaves of (slow-growing) evergreen land plants[77][78].

Duckweed is thus the only known plant that accumulates high levels of zeaxanthin in its photosynthetic organs while also growing very rapidly[76]. Duckweed may also be unique among dietary zeaxanthin sources in providing a particularly well-rounded cocktail of dietary factors that interact synergistically with zeaxanthin in opposing inflammation. Duckweed also has a high content of vitamin E[78][79] and phenolic antioxidants[80][81]. In addition, duckweed has a high ratio of inflammation-resolving omega-3 PUFAs to immunostimulatory omega-6 PUFAs (Figure 5; [82]).

In addition to taking advantage of duckweed’s exceptional propensity to accumulate zeaxanthin, it will be of interest to prevent post-harvest removal of zeaxanthin by suitable environmental conditions and/or natural or engineered mutants.

5.4. Performance under Elevated CO

2

Growth under the elevated CO2 levels, typical of a space cabin environment, was unimpaired in duckweed even under continuous very high light levels that lead to considerable carbohydrate build-up[76]. In contrast, other candidates of leafy vegetable species considered for use on the International Space Station, exhibited decreases in growth, leaf number and leaf area, and biomass under elevated CO2 concentrations[83]. The robustness of Lemnaceae may be related to (i) a relaxation of the controls on growth rate acting in land plants[84] and (ii) preferential use of nitrogen in the form of ammonium over nitrate. It is the use of nitrate as a nitrogen source that can enhance ROS production under elevated CO2[85]. The combination of high nitrate levels and elevated CO2 triggered premature senescence in land plants[28][30][86]. In terms of environmental controls on growth, most land plants quickly curb growth when water or nutrients begin to become limiting, and speed up the completion of the plant life cycle[26]. In contrast, Lemnaceae floating on water and with large nitrogen stores (in the form of storage protein) exhibited unabated growth across a wide range of environmental conditions irrespective of carbohydrate build-up under earth-ambient CO2 levels[77][78].

6. Conclusions

Here we identify the importance as well as the dangers of oxygen and the formation of ROS. Organisms need to maintain a delicate balance between antioxidants and oxidants to support redox homeostasis and signaling in support of growth, development, and stress protection. Some environmental conditions on earth have the potential to disrupt this delicate balance. Moreover, space environments expose plants and astronauts to additional disrupting stresses, such as space radiation in particular but also in addition to other conditions. Identification of plant species with superior rates of production of oxygen and essential human micronutrients as well as the removal of CO2 and recycling of human waste, are essential to the success of future long-term space missions (summarized in Figure 4). Plants of the family Lemnaceae have multiple traits that may help minimize the negative impacts of the combination of stressors encountered in space environments. Unlike land plants, Lemnaceae showed a stimulation, rather than inhibition, of growth under microgravity and exhibited relatively low sensitivity to elevated CO2. Lemnaceae’s exceptional antioxidant content may also reduce its sensitivity to GCR. These attractive genetic traits of Lemnaceae for space environments are features of the plants adapted to the unique aquatic environment.

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