Why is phosphorus-deficiency unusual in animals, and how are domestic bosts (Bos spp.) the exception that proves a rule?

@tonyrebelo @jeremygilmore @paradoxornithidae @matthewinabinett @charles_stirton @ludwig_muller @zarek

Please see:

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

https://epashupalan.com/10047/animal-nutrition/phosphorus-role-in-rumen-fermentation-process-in-ruminants/

Phosphorus (https://en.wikipedia.org/wiki/Phosphorus#:~:text=Phosphorus%20is%20an%20element%20essential,complex%20compounds%20fundamental%20to%20cells.) is an extreme nutrient, in being perhaps the most important element for Life, but not subject to deficiency in the ways familiar for many lesser nutrients.

In this Post, I attempt to explain how the only animals often described as 'deficient' in phosphorus, namely domestic bosts (Bos taurus and Bos indicus), are 'an exception that proves a rule'.

THE PUZZLE OF PHOSPHORUS: CRUCIAL BUT SELDOM DEFICIENT IN ANIMALS

Life on Earth is usually described as carbon-based (https://en.wikipedia.org/wiki/Carbon-based_life). However it could also be aptly described as phosphorus-based.

Phosphorus - an element far scarcer than carbon or nitrogen - is an indispensible component of the most basic molecules in organisms, around which genetics and metabolism revolve. I refer particularly to

• DNA (deoxyribonucleic acid, https://en.wikipedia.org/wiki/DNA), which is a phosphorus-based, polymer, and
• ATP (adenosine triphosphate, https://en.wikipedia.org/wiki/Adenosine_triphosphate), a relatively small molecule, which serves as the energy-currency of metabolism.

So, why is it that most Readers will not have heard of phosphorus-deficiency in the human body (https://en.wikipedia.org/wiki/Hypophosphatemia#:~:text=Hypophosphatemia%20is%20an%20electrolyte%20disorder,or%20softening%20of%20the%20bones.), or indeed the bodies of other organisms, in the sense familiar in the case of deficiencies of zinc (https://en.wikipedia.org/wiki/Zinc_deficiency), iodine (https://en.wikipedia.org/wiki/Iodine_deficiency), magnesium (https://en.wikipedia.org/wiki/Magnesium_deficiency), or calcium (https://en.wikipedia.org/wiki/Mineral_deficiency)?

Unlike phosphorus, silicon (https://en.wikipedia.org/wiki/Silicon) is superabundant in nature. Yet, deficiency of silicon, as manifested by soft/brittle fingernails, is more familiar than phosphorus-deficiency (https://editorial.victoriahealth.com/silica-supplements-for-hair-skin-and-nails#:~:text=As%20mentioned%20above%2C%20silica%20takes,encouraging%20healthy%20and%20strong%20nails.)

Has any Reader heard of buying an off-the-shelf supplement of phosphorus from a pharmacy or health store?

Given this framework, the aim of this Post is to figure out a puzzle: why is it only domestic bosts that are frequently described by veterinarians and livestock managers as phosphorus-deficient (https://www.mla.com.au/globalassets/mla-corporate/research-and-development/program-areas/livestock-production/20mla-phosphorus-8-page-brochure_apr2021_print.pdf)?

Phosphorus-deficiency in ruminants seems to make little sense, given that deer (large cervids) are so affluent in this element that they discard large quantities in their antlers (https://en.wikipedia.org/wiki/Antler), which they shed and regrow each year. Antlers, like bone, are composed mainly of calcium phosphate.

Perhaps the key to this puzzle is that what domestic bosts sometimes suffer from is shortage not in their own cells, but rather in the microbial cells in their guts, on which the whole mode of nutrition in ruminants depends.

RELATIVE CONCENTRATIONS OF PHOSPHORUS

Most of my facts come from Whitehead (2000, https://www.amazon.com.au/Nutrient-Elements-Grassland-D-Whitehead/dp/0851994377 and http://sherekashmir.informaticspublishing.com/381/1/9780851994376.pdf). However, the logic is my own.

First, let us trace phosphorus as it moves from soil, through plants, into animals such as livestock.

Soils in temperate zones usually contain 400-4000 mg/kg (= parts per million) of phosphorus, on a dry matter basis. This means that about one-fifth of one percent of the soil is phosphorus. Much of this is in the organic matter in soils.

The common fertiliser called superphosphate is, by comparison, 8-9% phosphorus, i.e. more than 40-fold richer than 'normal' soil.

The microbes in the soil contain about 1-2% phosphorus on a fresh matter basis. This would mean 5% on a dry matter basis, assuming that the water content of microbial cells is 70% water.

Mature herbage in pastures contains about 0.14% phosphorus (presumably on a dry matter basis), in roots and shoots alike. In fertilised pasture, the value can reach 0.8%.

Good-quality pasture contains 0.25-0.4% phosphorus, whereas unpalatable (fibrous) herbage contains <0.1%. Grasses and herbaceous legumes nave similar concentrations.

So, palatable herbage contains less than half a percent of phosphorus, even after being oven-dried.

Ruminants, eating this herbage, concentrate the phosphorus 5-10-fold in their bodies.

The ruminant body (excluding gut contents) is 0.7-1.0% phosphorus on a fresh mass basis. This means about 2.8% on a dry matter basis, assuming that water is 70% of the body.

(The corresponding value for the human species (including gut contents) is 3.3% (https://en.wikipedia.org/wiki/Composition_of_the_human_body).)

Of this, about 85% is in the skeleton and teeth. Indeed, the very mineral of which bone is composed, viz. apatite, is composed of the simple compound, calcium phosphate. On the basis of https://www.mdpi.com/1660-4601/16/4/525, I infer that the concentration of phosphorus in bone is at least 5%, on a dry matter basis.

This means that the ruminant body has managed to concentrate phosphorus six-fold, even where the pasture was phosphorus-rich by the standards of plant matter. This concentration is so efficient that the animal can afford to relegate most of its content of phosphorus to a mere building material, as opposed to the vital stuff of the cell nucleus and the mitochondria.

(Re-calculating this to check: if we take pasture to contain 0.4% phosphorus, and the ruminant body to contain 70% water, then we get a concentration of 2.66% in the animal (dry matter basis), which means that phosphorus has been concentrated 6.7-fold by herbivory.)

Urine is poor in phosphorus. Most of the excreted phosphorus is in faeces, which have value as fertiliser partly for this reason.

"The concentration of P in the faeces of grazing animals is normally greater than that in herbage being consumed. With sheep grazing poor quality pasture, the concentration in faeces (0.4-0.7% P) was between two and four times greater than the concentration in herbage" (Whitehead, 2000).

More generally, the faeces of ruminants usually contain 0.5-1.5% phosphorus on a dry matter basis, which compares with about 0.1-0.5% in their food.

The milk of bosts contains about 1% of phosphorus, on a dry matter basis, assuming that the water content of milk is 90%(http://milkfacts.info/Nutrition%20Facts/Nutrient%20Content.htm and https://www.davita.com/diet-nutrition/articles/advice/top-low-phosphorus-foods-for-a-healthy-kidney-diet#:~:text=Milk%20and%20milk%20products%20are,%2C%20such%20as%20calcium%2Dphosphate.).

Phosphorus is absorbed only in the small intestine. Nonetheless, ruminants extract most of the phosphorus from their food (75-85% in the case of adult bosts eating pasture, Whitehead, 2000). The fermentation of fibre in the rumen, which is the central feature of ruminants, is not essential for the extraction of phosphorus, most of which is not in the cell-walls that the microbes digest.

In ruminants, much of the phosphorus is recycled in saliva - promoting gut microbes that would otherwise not be able to operate rapidly enough on the basis of the phosphorus contained in the food. The saliva of bosts contains 370-720 mg per litre of phosphorus. Assuming that the water content of saliva is 90%, this means about 0.5% of phosphorus on a dry matter basis.

In summary, so far:

The concentrations of phosphorus, on a dry matter basis, are approximately

• soil 0.2%
• herbage 0.2%
• soil microbes 5%
• rumen microbes ?5%
• bone ?5%
• ruminant tissues (including skeleton) 3%
• ruminant tissues (excluding skeleton) ?0.5%
• saliva 0.5%
• faeces 0.5%
• milk 1%.

Please note that the concentration of phosphorus

• is about the same in herbage and the soil on which it grows, viz. 0.2%,
• is about the same in saliva, faeces, and the non-skeletal part of the ruminant body, viz. 0.5%,
• is about the same in microbes and bone, viz. 5%,
• is increased 15-fold from herbage to the whole body of the ruminant, and
• is twice as great in microbes as in the whole body of the ruminant.

MY INTERPRETATION

The basic reasons why phosphorus-deficiency is rare in animals are that

• this nutrient is so basic to the function of cells that there is minimal leeway; the animal tissues need to contain enough phosphorus to function, in the first place, and
• herbivores greatly concentrate phosphorus in converting green matter into their bodies.

Large ruminants are among the few animals in which phosphorus 'deficiency' is known, and this is only in the context of farming. I infer that this is likely to be a shortage for the microbial mass in the rumen (forestomach, which is essential for the fermentative digestion of fibre), rather than for the actual tissues of the animal.

When the microbes in the rumen are 'sufficient' in phosphorus for the fermentation of fibre, then the ruminant body is affluent in this nutrient to the point of superfluousness. Thus, deer can afford to allocated phosphorus to their deciduous head-adornments.

However, what is special about domestic bosts is that - more than any other domestic mammal - they have been selectively bred for extreme performance in somatic growth and the production of milk.

The microbes in the rumen exceed the non-bone tissues of the ruminant tenfold, in concentrations of phosphorus.

The combination in domestic bosts of large body size, fibrous diet, and extreme productivity can boost the phosphorus-demands of the microbial biomass in the bovine rumen to the point that, in certain situations and on certain diets, this mutualistic biomass can function 'deficiently' in a sense.

Whereas the animals have been selectively bred, their microbial mutualists remain subject to natural constraints - one of which is the supply of phosphorus.

I infer that the concentrations of phosphorus shift as follows:

plant matter 0.2%, which produces gut microbial matter 5.0%, which produces mammalian matter 2.5%, plus milk 1%, plus faeces 0.5%.

This suggests that

• the fermentation process is the part of this chain that most demands phosphorus, and
• ruminants are unlikely to suffer deficiency of phosphorus in their own tissues.

The latter point is shown by the facts that

• the animals - even while growing - defecate much phosphorus, despite concentrating phosphorus 10-fold from their diet into their bodies and milk,
• much phosphorus is relegated to the skeleton, where it is largely 'wasted' w.r.t. metabolism, reproduction, and growth, and
• in the case of large-bodied deer, as much phosphorus may be discarded by males in the form of shed antlers as is suckled from females to support the growth of juveniles.

So, the solution to the puzzle may be as follows.

The domestic bost is that odd entity, an animal subject to 'deficiency' in phosphorus, because

• it has been selectively bred for extreme productivity,
• this productivity depends on extreme function of the microbial biomass in the rumen, as the microbial cells replicate and metabolise rapidly in digesting the fibrous food, and
• this in turn depends on the supply of phosphorus, directly in the food and indirectly in saliva.

Even in the case of the unicellular microbes, no cell is likely to be deficient, in the conventional sense, in phosphorus. Instead, the 'deficiency' is a failure of supply to keep up with demand at the level of the collective, i.e. the 'ecosystem' constituted by the animal and its mutualistic microbes.

Partly because the microbial cells depend on concentrations of phosphorus severalfold those in rapidly metabolising animal cells, the rate of replication and metabolism of a given kilogram of cells of the animal risks outstripping that of a corresponding kilogram of the microbial cells.

In conclusion:

The rule, I suggest, is that there is no real phosphorus-deficiency in animals in the sense of various other nutrient elements, in which there are considerable within-cell tolerances, and supplementation works by restoring optimal function to the cells of the animal body itself.

What is exceptional about domestic bosts is that their gastric mutualism with fibre-digesting microbes has, in some cases, been pushed so far beyond the normal limits that, far from enjoying the affluence of phosphorus seen in wild ruminants, they suffer from shortage.

However, crucial to understanding this shortage is that it occurs at the level of the animal-microbe 'ecosystem', not within the bodies of either the animal or the microbes.

Posted on June 18, 2023 07:00 AM by milewski