The Spooky Science of How Undead Spores Reanimate



a biologist at the University of California, San Diego has found that spores are either dead or alive, in a state of suspended animation meant to outlast inhospitable conditions that can persist for millions of years. The ‘mostly dead’ cell in a spore cell reviving when the surrounding environment becomes more conducive to survival, the biologist added. This could lead to search for life on other planets and methods of fighting dangerous spores, such as those that cause foodborne illness.




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Maggie Chen Here’s a spooky conundrum: Is a spore alive or dead?


Gürol Süel, a biologist at the University of California, San Diego, wouldn’t blame you if you voted for dead: “There’s nothing to detect: no heartbeat, no gene expression. There’s nothing going on,” he says.


But a spore might actually just be dormant—in a deep state of suspended animation meant to outlast inhospitable conditions that can persist for millions of years, until the day the spore “wakes up,” zombie-like, ready to grow. For years, the questions of how spores know when to reanimate, and how they actually do it, have been open ones. A new paper in Science by Süel’s group has helped fill in those blanks—and the answer could have ramifications for everything from the search for life on other planets to methods of fighting dangerous spores, such as those that cause foodborne illness.Spores are typically single cells with tightly packed innards that can create new organisms. While many plants produce them to spread their seeds, bacteria can also form spores during periods of extreme temperatures, dryness, or nutrient deficiency. The spore cell then essentially hibernates its way through tough times.


Süel’s group was intrigued by the concept of a “mostly dead” cell reviving when the surrounding environment becomes more conducive to survival. “It was clear how spores come back to life if you dump a bunch of good stuff on them,” like large quantities of nutrients, says Süel. Likewise, when the environment is extremely hostile (for example, if no water is available), spores will simply not germinate. But most environments, the team realized, are not so black and white. For instance, “good” signals, like the presence of the nutrient L-alanine, might appear intermittently, then vanish. Would a slumbering spore be able to sense and process such a subtle hint?


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Getting an accurate read on its surroundings is important for the spore, because it would be a waste to expend the energy needed to wake up and germinate in an unfriendly environment. That could stymie successful growth, or even lead to death. “You need to come back to life with nice timing, because otherwise you throw away your nice dormancy,” says Kaito Kikuchi, a previous student in Süel’s laboratory and a study coauthor. “You want to make sure you’re throwing away your protections when, and only when, the environment is good enough.” First, the scientists needed to identify which biological processes the spores could use while they were still hibernating. These processes could not use ATP (adenosine triphosphate, or cellular energy) or rely on cellular metabolism (for example, breaking down sugars), since those mechanisms are shut down during dormancy.

周囲で正確な読み物を取得することは、胞子にとって重要です。なぜなら、それは、非友好的な環境で目覚めて発芽するのに必要なエネルギーを消費するのは無駄だからです。それは成功の成功を妨害したり、死に至ることさえあります。「あなたは素敵なタイミングで生き返る必要があります。そうでなければあなたはあなたの素敵な休眠を捨てるので、あなたはあなたの素敵な休眠を捨てるからです」と、Süel’sLaboratoryの以前の学生であり研究の共著者であるKaito Kikuchiは言います。「環境が十分に良いときにのみ、あなたがあなたの保護を捨てていることを確認したいのです。」第一に、科学者は、胞子がまだ冬眠中に使用できる生物学的プロセスを特定する必要がありました。これらのプロセスは、ATP(アデノシン三リン酸、または細胞エネルギー)を使用したり、細胞代謝(たとえば、糖を分解する)に依存したりすることはできませんでした。

But, the researchers hypothesized, there was an alternative method: The spores might be able to sense small cumulative changes in their environment, until enough signals build up to trigger a sort of wake-up alarm. The mechanism that would induce these changes would be the movement of ions out of the cell—specifically, potassium ions.


These movements can be triggered by positive environmental signals, like the presence of nutrients. When the ions travel out of the cell thanks to passive transport, they generate a difference in potassium concentration inside versus outside the cell. This concentration difference allows the spore to store potential energy. Over time, as the spore continues to sense more positive signals, more ions would move out of the cell. This would also create a corresponding drop in potassium levels, as the ions exit. Eventually, the potassium content in the spore would lower to a certain threshold, signaling that it is safe for the cell to wake up. That would trigger reanimation and germination. In other words, says Süel, the spore essentially acts similar to a capacitor, or a device that holds electrical energy. “A capacitor is basically an insulator separating the concentration gradient of charges,” he says. “You can really store a lot of energy in this way, because the cell’s membrane is very thin.” Boone Ashworth Matt Burgess Matt Jancer Khari Johnson If this concept sounds familiar, that might be because nature has already used it in another branch of biology: This is similar to how a brain neuron fires. Sodium ions stream into the neuron, causing the cell to become positively charged. Once the charge threshold is reached, an action potential is triggered and the neuron discharges. Potassium ions then stream out of the cell, bringing it back to its resting state.

これらの動きは、栄養素の存在のような正の環境シグナルによって引き起こされる可能性があります。イオンがパッシブ輸送のおかげで細胞から移動すると、細胞内と内部のカリウム濃度に違いが生じます。この濃度の違いにより、胞子はポテンシャルエネルギーを保存できます。時間が経つにつれて、胞子がより陽性のシグナルを感知し続けるにつれて、より多くのイオンが細胞から移動します。これにより、イオンが出るにつれて、カリウムレベルの対応する低下も生成されます。最終的に、胞子のカリウム含有量は特定のしきい値まで低下し、細胞が目覚めるのは安全であることを示しています。それは復活と発芽を引き起こすでしょう。言い換えれば、胞子は本質的にコンデンサ、または電気エネルギーを保持しているデバイスに似た作用します。 「コンデンサは基本的に、電荷の濃度勾配を分離する絶縁体です」と彼は言います。 「細胞の膜は非常に薄いため、この方法で多くのエネルギーを保存できます。」ブーン・アシュワース・マット・バージェス・マット・ジャンサー・カリ・ジョンソンこの概念がおなじみのように聞こえるなら、それは自然がすでに生物学の別の分野でそれを使用しているからかもしれない。これは脳ニューロンが発射する方法に似ている。ナトリウムイオンはニューロンに流れ込み、細胞が正に帯電します。電荷のしきい値に達すると、活動電位が引き起こされ、ニューロンが排出されます。その後、カリウムイオンは細胞から流れ出て、その安静状態に戻します。

To test their hypotheses, the scientists developed a mathematical model based on equations that describe how neurons fire—then adapted them to predict how the movement of potassium ions could trigger spore germination. To clarify the role these ions play, the scientists modeled a spore strain that lacked a critical unit in the potassium importer that transports ions into the cell. If germination is triggered by potassium dropping below a certain threshold, they theorized, spores with a broken import pump would bloom faster, because they would have fewer of those ions.


That idea worked in a mathematical model, but they wanted to test it in real life. So the scientists genetically engineered spores of the bacteria Bacillus subtilis so that the pump would not work. Then, they applied a timed dose of the nutrient L-alanine to them and monitored their germination. Forty-two percent of the mutated spores bloomed, compared with only 5 percent of normal ones that were used as a control. “We see that if you knock out the pump, and they don’t have enough potassium inside the spore, they are much more trigger happy and germinate,” Kikuchi says—proving their prediction correct.


Next, the scientists wanted to measure how each dose of nutrients changed the electrochemical potential inside the spore. Their mathematical model had predicted that each dose would increase a spore’s negative electrochemical potential in a step-like pattern. If each dose given to the real spores led to a predictable step up, that would support the team’s hypothesis that the cell uses its electrochemical potential to measure the friendliness of its environment, as a cue for when it’s safe to reanimate.


To visualize this with the Bacillus subtilis spores, the scientists mixed a positively charged fluorescent dye into the liquid surrounding them. The dye stuck to the spores, and the more negatively charged they became, the more dye would attach. So by measuring the spores’ fluorescence, the scientists could quantify how negatively charged each one was. When this fluorescence was graphed over time, a step-like pattern emerged that corresponded to each dose of nutrients—once again proving the prediction correct.


“This work has real potential to give us a whole new handle—specifics—on how germination proceeds,” says Peter Setlow, a spore scientist at the University of Connecticut who was not involved in the study. And that has some real-word use cases, he says, because spores can also be “causative agents for all kinds of nasties.” For example, certain bacterial spores can bury themselves in food, causing major illness when ingested. Germinating spores are much easier to get rid of than dormant ones, because they have shed their protections against chemicals and extreme temperatures. As a result, figuring out how spores wake up may provide insights into how to kill them if needed, Setlow says.

「この作品には、発芽がどのように進行するかについて、まったく新しいハンドル、特異的なものを提供する本当の可能性があります」と、コネチカット大学の胞子科学者であるPeter Setlow氏は述べています。そして、胞子は「あらゆる種類の厄介な人の原因となるエージェント」になる可能性があるため、いくつかの実際のユースケースがあると彼は言います。たとえば、特定の細菌の胞子は自分自身を食物に埋めることができ、摂取時に大きな病気を引き起こす可能性があります。発芽胞子は、化学物質や極端な温度に対する保護を流しているため、休眠胞子よりもはるかに簡単に取り除かれます。その結果、胞子がどのように目を覚ます方法を理解することで、必要に応じてそれらを殺す方法についての洞察を提供する可能性がある、とSetlowは言います。

Better understanding of spore dormancy could very well provide insights into new creatures that may seem dead but are not—like potential lifeforms on other planets. In a place like Mars, where the environment is dusty and seemingly barren, sources of life would most likely resemble spores—hidden somewhere cozy, waiting for signals to come back to life. “We’re not going to find a green man walking around,” says Süel. “If anything left is still somewhat alive, it’s probably going to be something like a spore that can survive the hostile environment that Mars has been for the past few millions of years.” Agata Zupanska, a space plant biologist at the Search for Extraterrestrial Life (SETI) Institute who was not involved in the study, agrees. “I would expect that martian bacteria, if they were there, would likely evolve a similar mechanism,” she says. “Dormancy is good. Evolutionarily, it is very successful.” She calls spores “a fascinating solution to surviving bad environmental conditions—you have a choice: You can either die or become dormant.” This work, she says, answers the question of “how something with no molecular and energetic tools can monitor the environment and respond to persistently good conditions.” Before scientists search for spores on Mars, there’s still a lot to do on Earth. Süel wants to keep studying how ions affect major processes in the spore. He thinks that while many biologists focus on gene expression or cell metabolism, something more passive, like the energy generated from ion gradients, could lead to surprising new discoveries. “If we can understand extremely dormant cells on our planet, maybe it’ll give us a better understanding of what to expect” when searching for life in the rest of the universe, Süel says.

胞子の休眠をよりよく理解することは、他の惑星の潜在的な生命体など、死んでいるように見えるかもしれないがそうではない新しい生き物への洞察を非常によく提供することができます。環境がほこりっぽく、一見不毛の場所である火星のような場所では、生命の源は胞子に似ている可能性が最も高いでしょう。 「私たちは緑の男が歩き回っているのを見つけるつもりはありません」とスエルは言います。 「残っているものがまだいくらか生きている場合、それはおそらく、火星が過去数百万年間であった敵対的な環境を生き残ることができる胞子のようなものになるでしょう。」研究に関与していない地球外生命(SETI)研究所の検索の宇宙工場生物学者であるアガタ・ズパンスカは同意します。 「火星のバクテリアがそこにいたら、同様のメカニズムを進化させる可能性が高いと思います」と彼女は言います。 「休眠は良いです。進化的に、それは非常に成功しています。」彼女は胞子を「悪い環境条件を生き残るための魅力的な解決策です。あなたには選択肢があります。死ぬか休眠することができます。」この仕事は、「分子およびエネルギーのあるツールがないものが環境を監視し、永続的に良い状態に応答することができる方法」という質問に答えていると彼女は言います。科学者が火星で胞子を探す前に、地球上でやることがたくさんあります。 Süelは、イオンが胞子の主要なプロセスにどのように影響するかを研究し続けたいと考えています。彼は、多くの生物学者が遺伝子発現または細胞代謝に焦点を合わせているが、イオン勾配から生成されたエネルギーのように、より受動的なものは驚くべき新しい発見につながる可能性があると考えています。 「私たちの惑星で非常に休眠した細胞を理解できれば、宇宙の残りの部分での生活を探すとき、それは私たちに何を期待すべきかをよりよく理解することができるかもしれません」とSüel氏は言います。