The Phosphorus Cycle: Cause or Effect?

"Life would be impossible without phosphorus," begins an editorial in Nature.

Present in molecules from DNA to membrane lipids to the compounds that shuttle energy in cells, it acts as an essential nutrient alongside nitrogen. Phosphorus moves through the environment in vigorous biogeochemical cycles, reflecting its chemical reactivity and intense competition by hungry organisms. [Emphasis added.]

How did this bio-geo-chemical cycle begin? Scientists at the University of Cambridge are perplexed about "How life and geology worked together to forge Earth's nutrient rich crust." In their analysis, they see that the element phosphorus appears to have increased in the crust around the same time as the Cambrian explosion. Was one the cause or the effect of the other? It didn't seem coincidental.

Around 500 million years ago life in the oceans rapidly diversified. In the blink of an eye — at least in geological terms — life transformed from simple, soft-bodied creatures to complex multicellular organisms with shells and skeletons.

Now, research led by the University of Cambridge has shown that the diversification of life at this time also led to a drastic change in the chemistry of Earth's crust — the uppermost layer we walk on and, crucially, the layer which provides many of the nutrients essential to life.

They reiterate, as we’ve discussed before, that phosphorus (P) is a limiting factor on biological productivity. Unlike the other most abundant vital elements (C, H, O, N, S), P must be extracted from rocks by chemical weathering — not in its pure form, which is explosive, but as PO43- (phosphate). Microbes and plants can utilize inorganic phosphate (Pi). Then other organisms can use the phosphate-containing molecules made by them (organic phosphate, or Po).

Craig Walton of Cambridge points out that once life became abundant in the oceans, a phosphorus recycling program could begin.

When these organisms die, most of the phosphorus is returned back into the oceans. This efficient recycling process is a key control on the amount of total phosphorus in the ocean, which in turn supports life, "It enables us to have all the life we see around us today, so understanding when this process started is really key," said Walton.

The Oxygen Theory for the Cambrian Explosion plays into his model, although he does not explicitly say he believes oxygen caused the sudden increase in animal life. He only points out the interesting correlation.

But, all of this biological reprocessing power relies on oxygen. This is what fuels the bacteria responsible for the breakdown of dead organic material that returns phosphorus back into the oceans.

The researchers think that a surge in oxygen at around the time of the Cambrian explosion might explain why phosphorus increased in rocks. "If oxygen did increase at that time, then more oxygen may have been available to break down deep sea biomass and recycle phosphorus to shallow coastal regions," said Walton. Moving this phosphorus back towards the land meant it was better preserved in rocks that make up the continents."That series of changes were ultimately responsible for fuelling the activity of complex life as we know it," said Walton.

Oxygen, therefore, is a third essential component in the phosphorus cycle.

"It's tricky to unravel the sequence of events — whether complex life evolved in part because of increased supplies of oxygen and phosphorus to start with, or if they were in fact fully responsible for increasing availability of both, is still a controversial topic." Walton and the team now looking to investigate the trigger for and timing of this phosphorus enrichment in the crust in more detail.

Summing up, there is a remarkable interplay of biology with two abiotic elements (oxygen and phosphorus) that sustains life on our planet. The Cambridge scientists were unable to decide which came first, how the cycle was triggered, and how things stayed in balance once the cycle was initiated.

Organisms have remarkable mechanisms for dealing with phosphate limitation, as noted here. The Nature editorial blames man for messing up the cycle by mining phosphorus for fertilizer, which often drains into the oceans, causing toxic algal blooms.

The modern phosphorus cycle has been profoundly meddled with by humans to overcome phosphorus limitation. Half of the phosphorus available to crops in agricultural soils may come from fertilizer application. Fertilizer is a limited resource — often derived from ancient rocks composed of detritus deposited beneath marine upwelling zones — and its depletion will eventually lead to problems for agriculture and other organisms that rely upon it.

In March, Science Magazine featured Dan Egan's book about phosphorus, The Devil's Element and a World Out of Balance, "an enjoyable, lively, and thought-provoking read" according to reviewer Robert W. Haworth, an expert on phosphorus and the environment. Wise management of this critical element will be essential, as phosphate runoff can pollute waterways and deplete soils if handled carelessly. Yet its automatic recycling through the crust and biosphere is not mentioned in the review. If the world is "out of balance" now due to human activities, how did it get into balance in the first place?

A commentary by Senjie Lin in Nature Communications explores the complexities of biological responses to phosphorus limitation, including interactions with ocean acidification, climate, and nitrogen fixation. Lin leaves more questions than answers, but notes that phytoplankton differ in their responses to pH, so much more research is needed.

One particularly interesting finding about phosphorus comes from research on fruit flies. A new organelle was found in the intestinal cells of the flies that buffers phosphate to maintain homeostasis. Described by Gemma Conroy in Nature, this "previously unknown" organelle "acts like a reservoir of phosphate, helping to regulate levels of the nutrient inside cells and triggering processes that maintain tissues when it is in short supply."

Conroy tells how Charles Xu of Rockefeller University noticed some oval-shaped structures surrounded by multiple membranes that were being traversed by a phosphate-sensing transporter protein named PXo:

"These were quite visible, and we wondered what they were," says Xu. When the scientists took a closer look at the mysterious structures, they saw they had several membrane layers, and the PXo protein was transporting phosphate across them. Once inside the unfamiliar organelles, the phosphate was converted to phospholipids, the main building blocks of cellular membranes.

When the fly cells were deprived of phosphate, the organelles broke apart and released the stored phospholipids into each cell, indicating that they function like reservoirs, says Xu.

His team's paper in Nature shows microphotographs of these "PXo bodies" and describes how they store and release inorganic phosphate (Pi).

In unicellular organisms, Pi is indicative of environmental nutrient abundance and generally supports cell growth and division1. In metazoans, however, Pi availability is affected by nutrient uptake, systemic metabolism and local Pi usage, thus implicating more complex Pi signalling. In this study, we demonstrated that Pi starvation or PXo deficiency induces hyperproliferation and enterocyte differentiation in the epithelium of the Drosophila midgut, which might be a compensatory mechanism to produce more enterocytes capable of Pi absorption. Given the scarcity of knowledge about cytosolic Pi regulation in animal cells, our findings might have broad implications and open new avenues for studying Pi metabolism and signalling.

The system for just-in-time delivery of phosphates from a reservoir equipped with a sensor is reminiscent of our story about the way cells buffer and deliver heme.

The Cambridge article says that "life and geology worked together to forge Earth's nutrient rich crust." From a materialist perspective, that's a fallacy of personification. Mindless entities do not work together to forge something like a Cambrian animal body plan or a cell organelle with a sensor able to buffer phosphate for just-in-time delivery.

Scientists are generally wary of explanations that depend on lucky coincidences. In the phosphorus cycle, biology and geology are seen cooperating as to timing, triggers, balance, and homeostasis of essential parts for a functioning biosphere. These are concepts rich with purpose. If a functioning biosphere was intended, then these observational realities would make sense.