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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, 328 (2017). 2. P. Remigi, J. Zhu, J. P. W. Young, C. Masson-Boivin, Trends

Microbiol. 24, 63 (2016). 3. Z. Bozsoki et al., Science 369, 663 (2020). 4. F. Maillet et al., Nature 469, 58 (2011). 5. A. Genre et al., New Phytol. 198, 190 (2013). 6. P. Lerouge et al., Nature 344, 781 (1990). 7. T. V. Nguyen et al., BMC Genomics 17, 796 (2016). 8. K. R. Cope et al., Plant Cell 31, 2386 (2019). 9. S. De Mita, A. Streng, T. Bisseling, R. Geurts, New Phytol.

201, 961 (2014). 10. Z. Bozsoki et al., Proc. Natl. Acad. Sci. U.S.A. 114, E8118

(2017). 11. C. Gibelin-Viala et al., New Phytol. 223, 1516 (2019). 12. F. Feng et al., Nat. Commun. 10, 5047 (2019). 13. L. Rutten et al., Plant Physiol. 10.1104/pp.19.01420

(2020), 14. R. van Velzen, J. J. Doyle, R. Geurts, Trends Plant Sci. 24,

49 (2019).

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: kbuesseler@whoi.edu

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 12.35

14C 2000 10,000 5730

99Tc 1000 10,000 211,000

125Sb 800 1000 2.77

60Co 200 1000 5.27

106Ru 100 100 1.01

137Cs 90 100 30.0

134Cs 60 100 2.06

90Sr 30 100 29.1

129I 9 100 16,000,000

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.

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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, 173 (2017). 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, 11092 (2017).

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, 1289 (2019). 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); https://www4.tepco.co.jp/en/sp/ decommission/progress/watertreatment/images/ tankarea_en.pdf.

10. Our Radioactive Ocean, www.ourradioactiveocean.org.

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.abc1507

10,000,000

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10,000

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10,000

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50% 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 × 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).

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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.

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Opening the floodgates at Fukushima Ken O. Buesseler

DOI: 10.1126/science.abc1507 (6504), 621-622.369Science

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