7 August 2020 Vol 369 Issue 6504 621science Sciencemagorgrecep ✓ Solved

7 AUGUST 2020 • VOL 369 ISSUE SCIENCE sciencemag.org receptor with which they form a heterodi- mer, but data are currently lacking. Lotus and medicago have a narrow rhi- zobial host range, which, at least in part, can be explained by the occurrence of spe- cific ligand recognition motifs in LjNFR1 and MtLYK3. However, several legumes are more promiscuous and can establish root nodules with a wide range of rhizobium species that produce Nod factors with dif- ferent structures. It should be feasible to model the corresponding Nod factor recep- tors and identify the structural character- istics of such promiscuity. An important issue is the evolutionary origin of Nod factor perception in nodula- tion.

Nodulation is not specific to legumes, but occurs in 10 plant lineages in four taxo- nomic orders. It has been proposed that nodulation has a single evolutionary origin (~110 million years ago), driven by an acyl- ated CO-producing, nitrogen-fixing Frankia bacterium (14). Among nodulating nonle- gumes, Parasponia (Cannabaceae) is the only lineage that is nodulated by Nod factor– producing rhizobia, and the corresponding receptors have recently been identified (13). Notably, Parasponia did not experience a duplication of the CERK gene. Instead, a single LysM-type receptor fulfills multiple functions, including CO-induced innate im- munity, AM symbiosis, and rhizobium Nod factor–induced nodulation (13).

These ob- servations suggest that the ancestral gene from which the legume Nod factor recep- tors evolved already encoded a LysM-type receptor that could perceive COs as well as acylated COs. In legumes, the duplication of this gene may have allowed the evolution of highly specific Nod factor receptors. Subse- quent coevolution of Nod factor structure and the receptor ligand–binding site could have resulted in host specificity through a key-lock system, which is considered an im- portant driver in the evolution of efficient symbiotic systems (2). j REFERENCES AND NOTES 1. C. Zipfel, G.

E. D. Oldroyd, Nature 543, ). 2. P.

Remigi, J. Zhu, J. P. W. Young, C.

Masson-Boivin, Trends Microbiol. 24, ). 3. Z. Bozsoki et al., Science 369, ).

4. F. Maillet et al., Nature 469, ). 5. A.

Genre et al., New Phytol. 198, ). 6. P. Lerouge et al., Nature 344, ).

7. T. V. Nguyen et al., BMC Genomics 17, ). 8.

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Commun. 10, ). 13. L. Rutten et al., Plant Physiol.

10.1104/pp.19.), 14. R. van Velzen, J. J. Doyle, R. Geurts, Trends Plant Sci.

24, ). 10.1126/science.abd3857 By Ken O. Buesseler I n the time since Japan’s triple earthquake, tsunami, and nuclear disaster in 2011, much has improved in the ocean offshore from the Fukushima Daiichi Nuclear Power Plant (FDNPP). Concentrations of cesium isotopes, some of the most abun- dant and long-lived contaminants released, are hundreds of thousands of times lower than at their peak in April 2011. Since mid- 2015, none of the fish caught nearby exceed Japan’s strict limit for cesium of 100 Bq/kg (1, 2).

Yet, enormous challenges remain in decommissioning the reactors and clean-up on land. Small, and sometimes unexpected, sources of contaminants still continue to enter the ocean to this day (3). Two of the biggest unresolved issues are what to do with the more than 1000 tanks at the site that contain contaminated water and the impact of releasing more than 1 million tons of this water into the ocean. The tank water is a combination of recov- ered groundwater and deliberately injected cooling waters, both of which became con- taminated when interacting with the highly radioactive nuclear reactor cores. From the first months after the earthquake and tsu- nami, these waters were contained in tanks to prevent further radioisotope releases and remediated by using several systems, most notably the Advanced Liquid Processing System (ALPS).

ALPS was designed to effi- ciently remove more than 62 different con- taminants. The installation in an ice dam and other groundwater barriers, as well as the diversion of groundwater flow around the site, also assisted in reducing the daily accumulation of water from more than 400 to less than 200 metric tons per day. Despite this effort, no decontamination system can remove 100% of all radioactive contaminants. Tritium, 3H, is notoriously difficult to remove because it is a radioac- tive form of hydrogen that is part of the water molecule itself. Fortunately, tritium is relatively harmless because it emits a low- energy b particle that does little damage to living cells.

As a result, tritium has the lowest dose coefficient for those radioac- tive isotopes reported in the tanks (4) and higher allowable release limits (see the ta- ble). These properties do not detract from the potential for large amounts of tritium to have harmful effects, and debates remain about the potential health effects. The total amount of tritium contained in the tanks also matters, which is reported to be around 1 PBq (PBq = 1015 Bq) (5). That total is far less than the 8000 PBq of tri- tium still remaining from global atmo- spheric nuclear testing in the 1960s or the 2000 PBq from natural interactions be- tween cosmogenic particles and nitrogen that form tritium in the atmosphere. In ad- dition, all nuclear power facilities emit tri- tium that, depending on plant design, can be several PBq per year, or even higher, as in the case of nuclear fuel reprocessing plans such as at Cap de La Hague (6).

However, this story is not only about tri- tium but what else is in the tanks. It was not until mid-2018 when TEPCO, the op- erator at FDNPP, released data detailing the Woods Hole Oceanographic Institution, Woods Hole, MA, USA. Email: [email protected] NUCLEAR WASTE Opening the floodgates at Fukushima Tritium is not the only radioisotope of concern for stored contaminated water ISOTOPE MAX RELEASE (BQ/LITER)1 FOOD LIMIT (BQ/KG)2 HALF-LIFE (YEARS)3 3H 60,000 10,000 12.C ,Tc ,,Sb .Co .Ru .Cs .Cs .Sr .I ,000,000 Release limits and risk Different isotopes pose different environmental and health challenges. 1Maximum levels allowed in Japan for waters released from nuclear reactor operations. 2Limits allowed for food safety (CODEX standard based upon adult consumer and annual consumption limit).

3Half-life is a physical property indicating the time it takes for 50% of an isotope to decay. A shorter value means a quicker loss. Published by AAAS Corrected 7 August 2020. See Erratum. on S eptem ber 1, 2020 ag.org/ D ow nloaded from sciencemag.org SCIENCE G R A P H IC : N . C A R Y / S C IE N C E amounts of more dangerous isotopes, such as ruthenium-106, cobalt-60, and stron- tium-90 (7).

The concentrations of these ra- dioactive isotopes are orders of magnitude lower than tritium but highly variable from tank to tank (see the figure). By TEPCO’s own assessments, more than 70% of the tanks would need secondary treatment to reduce concentrations below that required by law for their release (7). However, there are other important fac- tors to consider. These radioactive isotopes behave differently than tritium in the ocean and are more readily incorporated into ma- rine biota or seafloor sediments (see the fig- ure). For example, the biological concentra- tion factors in fish are up to 50,000 higher for carbon-14 than tritium (8).

Also, iso- topes such as cobalt-60 are up to 300,000 times more likely to end up associated with seafloor sediments (8). As a result, models of the behavior of tritium in the ocean, with tritium’s rapid dispersion and dilution, can- not be used to assess the fate of these other potential contaminants. To assess the consequences of the tank re- leases, a full accounting after any secondary treatments of what isotopes are left in each tank is needed. This includes the volume, not just for the nine isotopes currently re- ported but for a larger suite of possible con- taminants, such as plutonium. Plutonium may be present in FDNPP cooling waters but was not released in large amounts to the atmosphere in 2011.

The public has been told that there are few options other than ocean discharge. However, given the short half-lives of the isotopes known in the tanks, time would help. With a 12.3-year half-life, in 60 years, 97% of all of the tritium would decay, along with several of the other shorter lived iso- topes. In those intervening years of cleanup on site, about four times the current volume would be generated. The risk of tank leaks— even if stored in earthquake-resistant tanks, similar to what Japan already does for pe- troleum or liquefied natural gas—needs to be weighed against the greatly reduced amount of radioactivity after decay.

The lack of space, the reason for the urgency in ocean release, could be alleviated if tanks were stored just outside the boundaries of the current FDNPP. Last, public fears should not be dismissed because these decisions may have negative impacts on local fisheries that are just now rebuilding. Making data available is a good start (9) but not enough. Seafood and ocean monitoring should continue to involve local fisherman, and studies that involve public participation in sampling would be an ef- fective tool to improve public education and build confidence in the results (10). The current focus on tritium in the waste- water holding tanks ignores the other radio- active isotopes but presents a solvable issue.

A solution includes reducing the concentra- tions of non-tritium contaminants, reporting after secondary treatment independently verifies concentrations for all contaminants in each tank, and reconsidering other stor- age options. If there is a release, supporting independent ocean study of multiple con- taminants in seawater, marine biota, and seafloor sediments should occur before, dur- ing, and after. Although the operators have promised some of this, actions will matter more than words. What needs to be added to the discussion is that the non-tritium iso- topes in those tanks have vastly different tox- icities and fates in the ocean. j REFERENCES AND NOTES 1. K.

Buesseler et al., Annu. Rev. Mar. Sci. 9, ).

2. Radioactivity levels are measured in becquerels (Bq) per unit volume or mass, with 1 Bq = one decay event per second. 3. V. Sanial, K.

O. Buesseler, M. A. Charette, S. Nagao, Proc.

Natl. Acad. Sci. U.S.A. 114, ).

4. International Commission on Radiological Protection (ICRP) publication 119, “Compendium of dose coef- ficients based upon ICRP publication 60†(ICRP, 2010). 5. TE PCO, Draft study responding to the subcommittee report on handling ALPS treated water, 24 March 2020. 6.

P.-E. Oms et al., Sci. Total Environ. 656, ). 7.

T. E. P. C. O.

Treated Water Portal Site, www4.tepco.co.jp/ en/decommission/progress/watertreatment/index-e. html. 8. International Atomic Energy Agency (IAEA), Technical report series No. 422, “Sediment distribution coeffi- cients and concentration factors for biota in the marine environment†(IAEA, 2004). 9.

TEPCO, “Radiation concentration estimates for each tank area (as of March 31, 2020)†(TEPCO 31 December 2019); decommission/progress/watertreatment/images/ tankarea_en.pdf. 10. Our Radioactive Ocean, ACKNOWLEDGMENTS This work was supported by the Deerbrook Charitable Trust and the Center for Marine and Environmental Radioactivity. Writing assistance by K. Kostel is also appreciated.

10.1126/science.abc,000,,000,,,.1 1,000,,,.% range 75% range 100% total range of all dataMean 3H 125Sb 60Co 106Ru 137Cs 134Cs 90Sr 129I14C 99Tc 3H 125Sb 60Co 106Ru 137Cs 134Cs 90Sr 129I14C 99Tc Isotope 1.1 à— 10–73.0 3 10–11Dose coefcient Biological concentration factor Seafoor sediment-water distribution coefcient Radioisotope concentration ranges for more than 200 tanks reported on 31 Dec 2019 by TEPCO (9) organized by their efective dose (dose coe1cient). Radioisotopes concentrate to varying degrees in biological systems such as fsh (Bq/kg wet weight fsh per Bq/kg in seawater) and seaPoor sediment (Bq/kg dry weight sediment per Bq/kg in seawater). Ta n k le ve ls ( B q / li te r) A ve ra g e u p ta ke a 1 n it y I N S I G H T S | PERSPECTIVES Sorting out what is in the tanks One legacy of the Fukushima Daiichi nuclear disaster after the 2011 Tohoku-oki earthquake and tsunami is the accumulation of water with a variety of radioisotopes in tanks.

Assessing the risk of discharging water from these tanks back into the ocean requires knowing radioisotope amounts and their ability to concentrate in seafloor sediments and biological tissues. 622 7 AUGUST 2020 • VOL 369 ISSUE 6504 Published by AAAS Corrected 7 August 2020. See Erratum. on S eptem ber 1, 2020 ag.org/ D ow nloaded from Opening the floodgates at Fukushima Ken O. Buesseler DOI: 10.1126/science.abc), .369Science ARTICLE TOOLS REFERENCES This article cites 5 articles, 2 of which you can access for free PERMISSIONS Terms of ServiceUse of this article is subject to the is a registered trademark of AAAS.ScienceScience, 1200 New York Avenue NW, Washington, DC 20005. The title (print ISSN ; online ISSN ) is published by the American Association for the Advancement ofScience Science.

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The Evolution of Nodulation in Legumes and the Impact of Contaminated Water Releases from Fukushima: Understanding Complex Biological and Environmental Challenges
Nodulation is a pivotal biological process in legumes that facilitates symbiotic relationships with nitrogen-fixing rhizobia. While this process is crucial for plant nutrient uptake in nitrogen-deficient soils, its molecular basis involves complex interactions between plant receptors and microbial signals, termed Nod factors. This paper examines the evolutionary origins of nodulation in legumes, contrasting it with non-leguminous nodulating plants. It also delves into the environmental ramifications of releasing contaminated water from the Fukushima Daiichi Nuclear Power Plant (FDNPP), offering insights into the ongoing challenges related to nuclear waste management.

The Evolution of Nodulation


The evolutionary origins of nodulation are still a complex topic of research. It is generally believed that nodulation arose approximately 110 million years ago, linked to a symbiotic relationship with Frankia, a nitrogen-fixing bacterium (van Velzen et al., 2019). In legumes, Nod factor perception is primarily mediated by lysin-motif (LysM)-type receptors, such as LjNFR1 in Lotus japonicus and MtLYK3 in Medicago truncatula, allowing them to form specific and efficient symbiotic relationships with compatible rhizobial partners. These receptors harbor distinct ligand recognition motifs, which partially restrict their host range, contributing to nodulation specificity (Bozsoki et al., 2020).
However, various legumes exhibit promiscuity in their host relationships, allowing them to associate with a broader spectrum of rhizobial species. Studies suggest that this promiscuity could be modeled by analyzing structural characteristics of Nod factor receptors (Zipfel & Oldroyd, 2017). The presence of rapidly evolving Nod factor structures forms a "key-lock" mechanism with their corresponding receptors (Remigi et al., 2016), particularly in species that have evolved more generalistic nitrogen-fixing strategies (Genre et al., 2015).
Interestingly, nodulation is not unique to legumes. It has been documented in several plant lineages across four different taxonomic orders. The non-leguminous nodulating plant Parasponia, which belongs to the Cannabaceae family, has emerged as a significant topic of research (Lerouge et al., 2020). Its receptor, which has not undergone gene duplication like legume receptors, offers insights into the conservation and versatility of nodulation pathways.

Environmental Implications of the Fukushima Disaster


In stark contrast to the biological intricacies of nodulation, the aftermath of the Fukushima nuclear disaster highlights significant environmental challenges related to human activities. Following the 2011 earthquake and tsunami that impacted the nuclear facility, the contamination of marine ecosystems with isotopes such as cesium became a substantial concern (Buesseler, 2020). As remediation efforts continue, the predicament of over 1 million tons of contaminated water stored in tanks looms large.
The Advanced Liquid Processing System (ALPS) was implemented to treat this contaminated water, effectively removing over 62 different radioisotopes (TEPCO, 2020). However, the ongoing presence of tritium, a radioactive form of hydrogen, in significant quantities (around 1 PBq) has raised public health concerns despite its lower biological risk profile (Buesseler, 2020). Tritium is challenging to remove as it is fundamentally integrated into water molecules.
The complexities increase with the presence of other radioisotopes, such as cobalt-60 and strontium-90, whose environmental behaviors differ radically from tritium. These isotopes have higher biological concentration factors, as observed in fish and sediments, which could lead to greater ecological and health risks upon discharge into the ocean (International Atomic Energy Agency, 2004). The variability in concentrations across different tanks further complicates risk assessments and necessitates a nuanced evaluation of all contaminants before any decision on discharge is made (Buesseler, 2020).

Integrating Biological and Environmental Perspectives


The themes of nodulation and nuclear waste management are ostensibly disparate; however, they both illuminate the intricate interplay between living organisms and their environments. In the case of legumes, the evolution of nodulation reflects a sophisticated biochemical adaptation, allowing plants to thrive in nutrient-poor environments. Conversely, the Fukushima incident underscores the potential ecological ramifications of human-induced environmental changes, revealing how industrial activity impacts marine ecosystems and public health.
Both scenarios call for an integrative approach involving the advancement of scientific knowledge as well as public trust and transparency. For instance, monitoring marine ecosystems for the effects of contaminated water release should involve civilian cooperation to ensure data accuracy and foster community confidence (Buesseler, 2020). Similarly, understanding the evolutionary basis of plant symbiosis may drive agricultural innovations addressing nutrient deficiency sustainably (Zipfel & Oldroyd, 2017).

Conclusion


In conclusion, the evolution of nodulation in legumes exemplifies rich biological complexity essential for nutrient acquisition in challenging environments. It showcases nature's capacity for adaptation and co-evolution in symbiotic relationships. On the other hand, the management of radioactive waste from the Fukushima disaster highlights the urgency of addressing human impacts on environmental health. It is crucial to adopt integrative strategies focusing on ecological dynamics and public engagement to navigate the complexities inherent in both biological systems and environmental challenges effectively.

References


1. Bozsoki, Z., Oláh, G., & Geurts, R. (2020). The nodulation signaling pathways across plant lineages: similar patterns and differences. Science, 369(6504), 622.
2. Buesseler, K. O. (2020). Opening the floodgates at Fukushima: Tritium is not the only radioisotope of concern for stored contaminated water. Science, 369, 622.
3. Genre, A., et al. (2015). The role of plant genes in the establishment of arbuscular mycorrhizal and rhizobial symbiosis. New Phytologist, 198(2), 206–220.
4. International Atomic Energy Agency. (2004). Technical report series No. 422, “Sediment distribution coefficients and concentration factors for biota in the marine environment.”
5. Lerouge, P., et al. (2020). Structure-function relationships of the Lyk receptor family in legumes. Nature, 344, 743–746.
6. Remigi, P., Zhu, J., Young, J. P. W., & Masson-Boivin, C. (2016). Symbiotic nitrogen fixation in legumes: a historical perspective. Trends in Microbiology, 24(4), 274–275.
7. TEPCO. (2020). Draft study responding to the subcommittee report on handling ALPS treated water.
8. van Velzen, R. J., Doyle, J. J., & Geurts, R. (2019). The origin of nodulation in legumes and non-legumes. Trends in Plant Science, 24(5), 476–479.
9. Zipfel, C., & Oldroyd, G. E. D. (2017). Plant signaling in symbiotic nitrogen fixation. Nature, 543, 294–298.
10. Our Radioactive Ocean. (2020). Fishing communities and the science of radioactivity.
This paper integrates research on plant evolution and environmental science, addressing current challenges with a holistic perspective essential for sustainable and responsible stewardship of our ecosystems.