Not long ago I considered the element phosphorus as a test case for Michael Denton’s hypothesis of prior fitness of the environment for complex beings of our size. Phosphorus is a vital element on which life’s genetic and metabolic processes depend every picosecond. And yet P is not as easily cycled through the environment as are other elements like nitrogen and carbon. Phosphorus, therefore, can be considered a limiting factor for a productive biosphere. We left the issue as a work in progress, although ample circumstantial evidence exists that P bioavailability has not been a problem throughout Earth’s history (consider trilobites in an ancient ocean, sauropods in a tropical rain forest, or tropical fish in a lagoon consuming phosphorus with impunity in different eras).

Phosphorus has been in the news since that article. A paper in Nature admits that “the extent to which phosphorus availability limits tropical forest productivity is highly uncertain” because of intertwined effects with other limiting factors such as nitrogen. The authors experimented with adding phosphorus to a small patch of old growth rainforest in Amazonia, where soils are depleted in phosphorus. After two years, they saw increases in primary productivity, but not in stem growth. Disentangling the effects of phosphorus from other factors still seems uncertain.

At Charles University in the Czech Republic, two paleontologists investigated the phosphorus cycle over geological time by investigating the abundance of phosphatic marine shells in the fossil record as a proxy. In news from the Faculty of Science, they ascribe a transfer of phosphorus from shelly creatures to vertebrates in the Devonian:

M. Mergl laconically remarked that “phosphorus was stolen by vertebrates“. This remark actually became the “starting shot”. The question of the radical loss of phosphorus in the environment proved so exciting that both authors set about studying in detail the various corners of the cycle of this element. [Emphasis added.]

The Phosphorus Theory

Their tale begins with abundant phosphorus supporting the Ediacaran fauna. Then they attribute the Cambrian Explosion in part to still-plentiful phosphorus. 

The Early Paleozoic was a critical era of phosphorus cycle due to the intense involvement of biota in its dynamics. At the beginning, phosphorus was easily available in great amount and therefore many groups had the opportunity to build external phosphatic shells. This very likely contributed to the story of the Cambrian explosion, a period when representatives of almost all animal phyla appeared in the fossil record within a relatively short period of time. The Cambrian was thus a “golden age” for organisms with external phosphatic shells.

Like the oxygen theory, this explanation transfers the explanation for the origin of genetic information to the abundances of blind elements in the periodic table — hardly a logical idea. That would be like attributing the origin of books to the availability of movable type in a print shop with no Gutenberg. 

In Act Two of their biological opera, phosphorus divorced the shelly creatures and married the vertebrates. Marine shells declined in size because large phosphatic shells became a luxury. “This process has been accelerated by the emergence and evolutionary diversification of vertebrates, which, although they need a lot of phosphorus, are better at managing it,” the paleontologists surmise. But the plot thickens when anomalies emerge:

The subsequent era from the end of the Paleozoic to the present is characterized by limited but also selective availability of phosphorus in the seas and oceans. Geological processes such as the Variscan (400-300 Ma) and the Alpine orogenies (80 Ma to the present) have greatly aided the supply of phosphorus to the oceans.However, the ability of phosphorus to reach the oceans from its main source in the rocks of the denuded continents was hampered by the spreading of vegetation on land and other influences such as climate during this times [sic]. 

A Skeleton Key?

Climate change should not be used as a skeleton key for incomplete answers. In combination with “other influences,” storytellers can make any plot work. Kraft and Mergl published their ideas in an Opinion article, “Struggle for phosphorus and the Devonian overturn,” last month in Trends in Ecology & Evolution.

Most instructive is their proposal that “geological processes… have aided the supply of phosphorus” to the oceans and land. The role of volcanoes and orogenic processes in keeping phosphorus plentiful throughout Earth’s history deserves elaboration by design theorists. Consider what happened on January 14, when one of the most powerful volcanic eruptions ever recorded, the Hunga-Tonga volcano, surprised scientists with a massive plume visible from space (see the photo above). A new paper in Geophysical Research Letters reports a “massive phytoplankton bloom” that was visible from space as well following the eruption. 

Two independent bio-optical approaches confirmed that the phytoplankton bloom was a robust observation and not an optical artifact due to volcanogenic material. Furthermore, the timing, size, and position of the phytoplankton bloom suggest that plankton growth was primarily stimulated by nutrients released from volcanic ash rather than by nutrients upwelled through submarine volcanic activity. The appearance of a large region with high chlorophyll a concentrations less than 48 hours after the largest eruptive phase indicates a fast ecosystem response to nutrient fertilization. However, net phytoplankton growth probably initiated before the main eruption, when weaker volcanism had already fertilized the ocean.

Although chlorophyll itself does not contain phosphorus, the availability of phosphorus in the ash may have stimulated rapid proliferation of the plankton. 

Phosphorus Ecology

Does phosphorus availability impact predator-prey relationships? In a research article in PNAS, Guilloneau et al.investigated “Trade-offs of lipid remodeling in a marine predator–prey interaction in response to phosphorus limitation.” 

Microbial growth is often limited by key nutrients like phosphorus (P) across the global ocean. A major response to P limitation is the replacement of membrane phospholipids with non-P lipids to reduce their cellular P quota. However, the biological “costs” of lipid remodeling are largely unknown. Here, we uncover a predator–prey interaction trade-off whereby a lipid-remodeled bacterial prey cell becomes more susceptible to digestion by a protozoan predator facilitating its rapid growth. Thus, we highlight a complex interplay between adaptation to the abiotic environment and consequences for biotic interactions (grazing), which may have important implications for the stability and structuring of microbial communities and the performance of the marine food web.

The magical thinking in this story becomes evident when the authors opine that “marine microbes have evolved sophisticated strategies to adapt to P limitation” such as replacing phospholipids with non-P lipids. One must imagine microbes holding committee meetings, thinking out “strategies” as if they were business managers worried about maintaining their products under duress from shortages in the supply chain. “But if we do that,” one manager worries, “we become susceptible to organized crime.” 

The low availability of key nutrients like P in marine surface waters represents a grand challenge for microbes, particularly those inhabiting oligotrophic gyres. Although lipid remodeling enables these microbes to survive better in these potentially P-limited environments, as well as facilitating greater avoidance of ingestion by ciliate grazers, once ingested, these lipid-remodeled cells are unable to survive phagolysosomal digestion (Fig. 6). Therefore, these microbes face an unsolvable dilemma. 

The managers panic; what to do? Each option is potentially disastrous. “Thus, it is clear that adaptation to a specific niche can come with consequences to an organism’s viability,” the storytellers continue. Stay tuned for the next exciting episode! “…it remains to be seen what other trade-offs in predator–prey interactions exist following adaptation of cosmopolitan marine microbes to P limitation.”

Not Particularly Helpful 

Speculation like this is not particularly helpful in science, especially when the story is so evidence-starved as to depend on one single example of a microbe and its predator. “Global change is expected to exacerbate P limitation in the surface ocean due to water-column stratification accelerated by global warming,” they say at one point. Maybe that was the motivation to ensure their story got funded and published. But what do they know from their observations? And how can they extrapolate one predator-prey interaction to the whole globe?

Moreover, given that the effects of remodeling on predator–prey interactions we report here are ultimately controlled by in situ P concentrations (which controls lipid remodeling), then such interaction effects are also likely to be dynamic in their nature, given the often-seasonal nature of P limitation — e.g., in the Mediterranean Sea, PlcP-mediated lipid remodeling occurs across an annual cycle, whereby P limitation intensifies during spring and summer, but starts to become alleviated from September. Nonetheless, this work clearly highlights the complex interplay between the abiotic nutrient environment, microbes, and their grazers and how predator–prey dynamics are governed by abiotic control of prey physiology, which has important implications for how we model trophic interactions in marine ecosystem models, particularly in a future scenario where nutrient-deplete gyre regions are set to expand.

Readers should note that both predator and prey have not gone extinct, which would make a stronger case for P limitation in their limited ecological case.

Habitability Requires a Phosphorus Supply Chain

While agriculturalists worry about phosphorus for commercial fertilizers, none of these papers above suggest that the natural biosphere has ever suffered from a deficiency of phosphorus. The plankton bloom after the Tonga eruption shows how volcanoes can fortify marine environments with inorganic nutrients. Another paper in Nature Scientific Reports suggests that terrestrial environments, too, can take advantage of volcanic phosphorus. Pioneering plants can absorb phosphorus from volcanic ash and supply it to secondary growth through their leaf litter. This is interesting because many terrestrial soils contain volcanic ash containing insoluble inorganic phosphorus that was thought unavailable to plants. Volcanic islands like Japan and Hawaii, however, seem to have thriving ecosystems.

Despite volcanic ash soil covering about 20% of the land in Japan,and phosphorus deficiency being a serious problem in Japanese agriculture, net primary production in Japanese forests is primarily is not low compared to other temperate zones of the world. This suggests that natural vegetation on the infertile volcanic ash soil obtain sufficient nutrition including phosphorus.

Geology, therefore, appears to offer a supply chain for elemental nutrients built into our planet by means of plate tectonics coupled with thermodynamics — the availability of heat near the surface. Since a planet’s internal heat decreases over time, there may be temporal constraints on this supply chain. If so, one implication is that cold, dead worlds might not have a functioning biosphere even if they orbit in the habitable zone. Is Earth operating in a Goldilocks time as well as a Goldilocks location? These are good questions for design theorists to investigate. Meanwhile, Earth’s biosphere seems to be functioning tolerably with its natural phosphorus supply.