Seaweed can be used to “cook without rice”, so what is the “secret to making a meal”?

When it comes to absorbing carbon dioxide, many people think of forests. In fact, most of the carbon dioxide on Earth is absorbed by the ocean.

The ocean covers more than 80% of the Earth's surface and stores about 90% of the world's carbon dioxide, making it the largest active carbon reservoir on Earth. Marine vegetation absorbs and fixes carbon dioxide through photosynthesis, converts it into stable organic matter and stores it, forming a unique marine carbon reservoir called "Blue Carbon". Among them, the lush seagrass beds that are widely distributed in shallow seas from temperate to tropical regions are one of the main forces of marine carbon fixation.

However, this unique ecosystem has long puzzled scientists: where do the nutrients for the seagrass beds come from?

Farming requires fertilizers to achieve a good harvest, and seagrass beds also need nutrient support. However, most seagrasses grow in shallow marine environments that are nutrient-poor, especially nitrogen, which is the inorganic nutrient with the highest demand for plant growth.

In such a barren land, seaweed can thrive without any rice. There must be some unknown secret to its success.

Part 1

Pick up leaks, find a partner to get nitrogen... There are some tricks for plants to "eat dry rice"

Before introducing how seaweed obtains "nitrogen" nutrients in shallow sea environments, let us first look at how most green plants in nature obtain nitrogen.

Although the nitrogen content on the ground is high, most of it is inactive gaseous nitrogen, which plants cannot "eat". Gaseous nitrogen needs to be converted into several specific nitrogen-containing substances before plants can "eat" it. This process of "fixing" gaseous nitrogen is called "nitrogen fixation". Among them, some prokaryotic microorganisms (such as bacteria) can complete "biological nitrogen fixation". These microorganisms that can fix nitrogen are collectively called nitrogen-fixing bacteria. Under natural conditions, biological nitrogen fixation is the main way for the biosphere to retain nitrogen. Faced with such a precious resource, plants have a variety of ways to use it:

1. Secretly picking up nutrients from "free nitrogen-fixing bacteria"

Among the nitrogen-fixing bacteria, some free-living bacteria can be self-reliant: they fix nitrogen by themselves, find organic matter to eat by themselves, and "live like a team."

Previous studies have found that there are many such free nitrogen-fixing microorganisms in the bottom mud of seagrass beds, so people believe that seagrass mainly "picks up" from the environment and absorbs some of the "leftovers" of free nitrogen-fixing bacteria. However, such scattered nitrogen sources do not seem to be able to feed the lush seagrass beds, and the question has not been completely answered.

Seaweed can be used to "cook without rice", the secret of dry rice is exposed

Image source: Reference [5]

2. Symbiotic nitrogen fixation model with nitrogen-fixing bacteria

The work efficiency of autotrophic nitrogen-fixing bacteria is not high, and the amount of nitrogen fixed is also low. It is difficult for plants to rely on them alone. Therefore, some plants on land have developed a closer cooperative relationship with some fungi: the roots of plants have specialized structures that allow bacteria to "live" in their bodies like a "house". Plants provide food for bacteria, and bacteria fix nitrogen for plants.

The most well-known symbiotic nitrogen fixation model is between legumes and rhizobia. In the root nodule symbiosis, root cells come into close contact and incorporate the nodule nitrogen-fixing bacteria, forming round nodules that are highly efficient nitrogen-fixing factories.

Nodules on soybean roots:

Each nodule contains many rhizobia, forming an efficient terrestrial nitrogen fixation system.

(Image source: Reference [8])

3. Loose cooperation between plants and endophytes

Leguminosae plants develop nodules in order to cooperate with rhizobia, which is a difficult skill that most plants do not have. Therefore, some plants choose a simpler way to accommodate nitrogen-fixing bacteria: "opening" the bacteria's access to the roots and allowing the bacteria to live in the intercellular spaces or cell walls in the roots. However, plants will not specifically change the root morphology for this purpose, and no special structures will be produced.

These microorganisms that live in plants are collectively called endophytes. Some non-leguminous plants (such as sugarcane, wheat[2], and agave[3]) can recruit endophytes with nitrogen-fixing ability, which not only satisfies the need for nitrogen acquisition, but also does not require the preparation of special "houses" for bacteria, maintaining a loose association relationship, which is simple but not simplistic.

Endophytes in plants. This photo shows intracellular symbiotic bacteria in the roots of blue agave (Agave tequilana), which have nitrogen-fixing activity.

(Image source: Reference [3])

Land plants and microorganisms have a long history of cooperation. When the earliest plants evolved from algae in the ocean to land plants, they could not do without the help of microorganisms. After that, several small families of land plants chose to return to the ocean in the history of evolution and gradually adapted to the marine environment. This type of grass-like flowering plants that can live in the ocean are collectively called "seaweeds." Various seaweeds grow on shallow beaches like pastures on land, so they are called "seaweed beds."

Since land plants can form an intimate symbiotic cooperative relationship with nitrogen-fixing bacteria, do seaweeds, whose ancestors were once land plants, also have similar "social skills"?

Part 2

Seaweed: "Roots open wide" to welcome nitrogen-fixing bacteria

By studying Posidonia oceanica, a common plant in the Mediterranean, scientists have found clues to the mystery of the source of nitrogen fertilizer in seagrass beds: seagrasses also have a symbiotic nitrogen fixation system similar to that of terrestrial plants[4].

Oceanic seagrass is widely distributed in the Mediterranean region and is a landmark vegetation in the region. Because seagrass beds are more efficient at fixing carbon each year than an equivalent area of ​​the Amazon rainforest, its valuable ecological and cultural value has led UNESCO to list it as a World Heritage Site[6].

Seaweed Grass Field

(Image source: Reference [6])

Professor Marcel Kuypers' team at the Max Planck Institute for Marine Microbiology in Germany tracked the distribution of nitrogen in the seaweed and found that the roots of the seaweed can absorb gaseous nitrogen, and the fixed nitrogen will be transferred to the aboveground part. This pattern is particularly obvious in the summer growing season. This shows that there are indeed nitrogen-fixing bacteria in the roots of the seaweed! The symbiotic nitrogen-fixing system of land plants actually exists in the marine environment with completely different environmental properties. This is an unprecedented discovery.

Figure 1: Microbial nitrogen fixation in roots increased significantly in July and August, matching the peak growth season of plants. Figure 2: Changes in nitrogen transfer detected in plant leaves match the nitrogen fixation in roots, with more transfer occurring when nitrogen fixation is high (July).

(Image source: adapted from reference [4])

Scientists subsequently identified a new species of bacteria in the roots of the ocean seaweed: Candidatus Celerinatantimonas neptuna (Ca. C. neptuna) [7]. This bacterium is significantly correlated with the overall nitrogen fixation activity trend of the plant, and has a full set of nitrogen fixation genes, which can perform complete nitrogen fixation functions. Moreover, the "cooperative trade" between this bacterium and seaweed also completely follows the rules of cargo exchange in terrestrial nitrogen-fixing symbiosis: the bacteria exchange nitrogen with the plant and the plant exchange sugar with the bacteria. The cooperation model of the two systems is exactly the same.

Conceptual diagram of the interaction between endosymbiotic nitrogen-fixing bacteria and seagrass

The left side of the picture shows a cross-section of the root, in which the pink ones are nitrogen-fixing bacteria. The bacteria mainly colonize the cortical part of the plant root. The red arrows indicate that the bacteria absorb nitrogen and then provide ammonium salts to the plant; while the black arrows indicate that the plant provides sugar and the required oxygen to the bacteria.

(Image source: adapted from reference [4])

Under a fluorescent microscope, we can determine where the bacteria live: Ca. C. neptuna is distributed in the roots of seaweed, and the distribution location is closely related to the changes in nitrogen concentration in the roots. In the summer when growth is rapid, Ca. C. neptuna is still the dominant microorganism in the roots of seaweed; while in the roots of other seaweeds that do not show nitrogen fixation activity, this bacterium is almost not found.

The left image (d) shows the microbial environment in the roots under a fluorescence microscope. A large number of nitrogen-fixing bacteria (pink/blue) gather in the gaps between plant cell walls (green).

Figure e on the right is a tracer of nitrogen isotope concentration. The yellower the color, the more nitrogen there is, indicating that the nitrogen fixation process is more active.

Note the consistent association between bacterial clustering and nitrogen concentration shown by the white arrows across both graphs.

(Image source: adapted from reference [4])

Genetic analysis of Ca. C. neptuna also revealed that it is fully prepared for endosymbiotic life. For example, it can actively move to follow the footsteps of plants, recognize signals from plants, "shake hands and make peace" with the immune defense system of plants, and degrade pectin in cell walls to create a place to live. Many pieces of information show that this bacterium has a very similar lifestyle to nitrogen-fixing bacteria on land, and its endophytic characteristics are also the first to be found in marine microorganisms.

Part 3

What can we learn from the symbiotic nitrogen fixation between bacteria and seagrass?

The nitrogen-fixing cooperation between Poseidon and Ca. C. neptuna is like a replica of the cooperative relationship on land. The history of evolution always has echoes: perhaps when the ancestors of Poseidon returned to the ocean about 100 million years ago, away from their terrestrial microbial partners and "lonely and helpless", the ancestors of Ca. C. neptuna in the sea lent a hand to it. The completely different combination of species developed a similar cooperation model under similar difficulties. This pair of new friends opened up new territory in the impoverished seabed and wrote a new chapter.

The discovery of this new marine bacteria-seagrass endosymbiotic nitrogen-fixing system has also brought more opportunities and challenges. For example, how does seagrass recognize and accept this bacteria? Do other seagrasses (such as Zostera marina, which is more common in my country's waters) have similar symbiotic partners? What role do endophytic nitrogen-fixing bacteria play in the evolution of seagrass into the sea? How did the ancestors of seagrass complete the transformation from terrestrial symbiotic bacteria to marine symbiotic bacteria? The answers to these questions are waiting for scientists to reveal them one by one in the future.

In addition to in-depth academic discussions, the discovery of this symbiotic bacteria is also valuable for protecting the threatened seagrass bed ecosystem. At the same time, we may be able to develop some microbial "bacterial agents" based on this type of bacteria to consolidate the "blue carbon" inventory of seagrass beds, providing a new low-cost path to mitigate global change.

References:

[1] Blue Carbon: An Ocean Solution to Climate Change, China Climate Change Network. http://www.ccchina.org.cn/Detail.aspx?newsId=70773&TId=59

[2] Boddey, RM, Dobereiner, J. Nitrogen fixation associated with grasses and cereals: Recent progress and perspectives for the future. Fertilizer Research 42, 241–250 (1995). https://doi.org/10.1007/BF00750518

[3] Beltran-Garcia, M., White, Jr., J., Prado, F. et al. Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep 4, 6938 (2014). https://doi.org/10.1038/srep06938

[4] Mohr, W., Lehnen, N., Ahmerkamp, ​​S. et al. Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium. Nature (2021). https://doi.org/10.1038/s41586-021-04063-4

[5] Douglas G. Capone. A seagrass harbors a nitrogen-fixing bacterial partner. doi: https://doi.org/10.1038/d41586-021-02956-y

[6] Posidonia oceanica, Wikipedia,

https://en.wikipedia.org/wiki/Posidonia_oceanica

[7] Note: Celerinatantimonas is the genus name and neptuna is the specific epithet, the name of the Roman god of the sea. It is named so because its host plant, Neptune grass, is called Neptune grass in English. Candidatus is a "qualifier" in the nomenclature of prokaryotes, used to refer to species that have been identified by sequencing but not by pure culture.

[8] Image source: Iantcheva. A., Naydenova, G., 2020. Biological nitrogen fixation in legumes. Legume Hub. www.legumehub.eu, https://www.legumehub.eu/is_article/biological-nitrogen-fixation-in-legumes/

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Produced by: Gu Yuliang

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