Phosphorus Cycle K R M Mackey, Stanford University, Stanford, CA, USA a Paytan, University of California Santa Cruz, Santa Cruz, CA, USA

Phosphorus Cycle K R M Mackey, Stanford University, Stanford, CA, USA A Paytan, University of California Santa Cruz, Santa Cruz, CA, USA

Defining Statement Anthropogenic Alteration of the P Cycle: Eutrophication Introduction in Aquatic Ecosystems Microbially Mediated Processes Conclusion Genetic Regulation of Microbially Mediated Processes Further Reading

Glossary mineral formation Processes in which anions react assimilation (transitory immobilization) The process with cations in the environment to form insoluble of incorporating nutrients into cellular biomass. precipitates. authigenic Formed in situ rather than by having been mineralization The conversion of organic matter into transported or deposited in a location through simple inorganic compounds, primarily by microbial secondary processes. decomposition. chelation The reversible binding (complexation) of a nutrient limitation The cessation of photosynthetic ligand to a metal ion. biomass production in response to low availability of a diagenesis The process by which sediment physiologically important nutrient or nutrients. undergoes chemical and physical changes during its organic phosphorus A class of chemical compounds lithification. that comprises only those existing in or derived from eolian transport Advection of material via the living organisms. atmosphere or wind. orthophosphate Form of orthophosphoric acid

eutrophication Excessive nutrients in a body of water (H3PO4) in which three protons have been lost (i.e., 3– that cause a dense algal growth, followed by algal PO4 ); also called the phosphate anion. decomposition, anoxia, and impairment of the aquatic primary production The conversion of radiant or community. chemical energy into organic matter. immobilization The process by which labile productivity The rate at which radiant energy is used phosphorus is sequestered and removed from the by producers to form organic substances as food for environmental reservoir of reactive phosphorus for a consumers. period of time. solubilization The conversion of insoluble compounds inorganic phosphorus A class of chemical into soluble compounds. compounds that comprises those not existing in or weathering Processes by which rocks, minerals, and derived immediately from living organisms (e.g., soils get broken down through direct contact with the orthophosphate). atmosphere; can be physical or chemical.

Abbreviations PNP para-nitrophenyl phosphate ELF enzyme-labeled fluorescence Pst phosphate-specific transport PhoA alkaline phosphomonoesterase SRP soluble reactive phosphorus Pit phosphate transport system

Defining Statement phosphorus in the environment, microbially mediated transformations of phosphorus and their genetic regulation, This article includes a discussion of the global phosphorus and a discussion of microbial responses to anthropogenic cycle, including sources, sinks, and transport pathways of changes to the phosphorus cycle.

322 Environmental Microbiology and Ecology | Phosphorus Cycle 323

Introduction growth of producers, the phosphorus cycle contributes to the regulation of global climate. Phosphorus is an essential nutrient for all living organisms, In aquatic environments, photosynthetic microbes (i.e., and the phosphorus cycle is an important link between phytoplankton) may comprise a substantial portion of the Earth’s living and nonliving entities. The availability of photosynthetic biomass and hence primary production. phosphorus strongly influences primary production, the Marine and freshwater phytoplankton are characterized process by which photosynthetic organisms fix inorganic by extensive biodiversity, and as a group, inhabit an carbon into cellular biomass. Therefore, knowledge of the incredible number of different niches within aquatic phosphorus cycle is critically important for understanding environments. Phytoplankton, like other microbes, have the global carbon budget and hence how biogeochemical strategies that enable them to adapt to changes in the cycles impact and are influenced by global climate. amounts and forms of phosphorus available within their environment. For example, the production of phosphatase enzymes, which hydrolyze organic P compounds to inorganic phosphate, helps to mediate the mineralization of organic phosphorus compounds in surface waters and Global Significance of the Phosphorus Cycle allows cells to adapt when phosphate levels are low. Natural assemblages of microbes have a critical role in the Recent estimates suggest that phytoplankton are phosphorus cycle because they forge a link between phos- responsible for as much as half of global carbon fixation, phorus reservoirs in the living and nonliving environment. thereby contributing significantly to the regulation of Microbes facilitate the weathering, mineralization, and solu- Earth’s climate. Phytoplankton productivity is strongly bilization of nonbioavailable phosphorus sources, making influenced by nutrient availability, and which nutrient orthophosphate available to microbial and plant commu- ultimately limits production depends on (1) the relative nities and hence to higher trophic levels within the food web. abundance of nutrients and (2) the nutritional require- However, microbes also contribute to immobilization of ments of the phytoplankton. With some exceptions, phosphorus, a process that diminishes bioavailable phos- production in most lakes is limited by the availability of phorus by converting soluble reactive forms into insoluble phosphorus, whereas limitation of primary production in the ocean has traditionally been attributed to nitrogen, forms. The mechanisms of microbial involvement in these another nutrient required by cells in large quantities. processes vary from passive (e.g., resulting from microbial However, phosphorus differs from nitrogen in that the metabolic byproducts) to highly regulated active contribu- major source of phosphorus to aquatic environments is tions (e.g., the regulation of gene expression in response to the weathering of minerals on land that are subsequently environmental cues). introduced into water bodies by fluvial and aeolian Microbially mediated processes also link the phos- sources. In contrast, microbially mediated nitrogen phorus cycle to the carbon cycle and hence to global fixation, in which bioavailable forms of nitrogen are gen- climate. During photosynthesis, photoautotrophs incor- erated from nitrogen gas in the atmosphere, is a major porate phosphorus and carbon at predictable ratios, with pathway by which phytoplankton gain access to nitrogen approximately 106 carbon atoms assimilated for every (in addition to continental weathering). Because there is one phosphorus atom for marine photoautotrophs and no phosphorus input process analogous to nitrogen fixa- terrestrial vegetation. The phosphorus cycle therefore tion, marine productivity over geological timescales is plays an important role in regulating primary productiv- considered to be a function of the supply rate of phos- ity, the process in which radiant energy is used by phorus from continental weathering and the rate at which primary producers to form organic substances as food phosphorus is recycled in the ocean. Accordingly, the for consumers, as in photosynthesis. phosphorus cycle influences phytoplankton ecology, pro- Because phosphorus is required for the synthesis of ductivity, and carbon cycling in both marine and numerous biological compounds, its availability in the freshwater ecosystems. environment can limit the productivity of producers when other nutrients are available in excess. This fact carries important implications for the global carbon bud- Characterizing and Measuring Environmental get because the rate of incorporation (fixation) of carbon Phosphorus Pools dioxide into photosynthetic biomass can be directly con- Occurrence of elemental phosphorus in the environment trolled by the availability of phosphorus; if phosphorus is is rare, given that it reacts readily with oxygen and com- not available, carbon dioxide fixation is halted. The inter- busts when exposed to oxygen; thus phosphorus is section of the phosphorus and carbon cycles is of typically found bound to oxygen in nature. Phosphorus particular significance for global climate, which is affected has the chemical ability to transfer a 3s or p-orbital by atmospheric carbon dioxide levels. Hence, through the electron to a d-orbital, permitting a relatively large 324 Environmental Microbiology and Ecology | Phosphorus Cycle number of potential configurations of electrons around dissolved because it is associated with water molecules the nucleus of the atom. This renders the structures of homogeneously in solution rather than being held within phosphorous-containing molecules quite variable and a salt crystal.) By contrast, colloidal forms include relatively reactive. These properties are likely responsi- any tiny particles that are distributed evenly throughout ble for the ubiquity and versatility of phosphorus- the solution but that are not dissolved in solution. Soluble containing compounds in biological systems. phosphorus is commonly reported because colloidal Because phosphorus exists in many different physical phosphorus particles are very small, and differentiating and chemical states in the environment, specific definitions between colloidal and dissolved phosphorus is methodo- are needed to clarify different parts of the phosphorus pool. logically difficult. Chemical names reflect the chemical composition of the When living organisms assimilate phosphorus into phosphorus substance in question, whereas other classifica- their cells, the resulting phosphorus-containing com- tions are based on methodological aspects of how the pounds are collectively called ‘organic phosphorus’. It substance is measured. For example, ‘orthophosphate’ is a must be stressed that this definition of the biologically chemical term that refers specifically to a phosphorus atom associated phosphorus as ‘organic phosphorus’ is not iden- bound to four oxygen atoms – forming the orthophosphate tical to the chemical definition of organic compounds 3– molecule (PO4 , also referred to as phosphate), whereas the (e.g., containing carbon). For example, some intracellular term ‘soluble reactive phosphorus’ (SRP) is a methodologi- biologically synthesized compounds such as polypho- cal term referring to everything that gets measured when an sphate may not contain C bonding. The term organic orthophosphate assay is performed (such as the ascorbic acid phosphorus encompasses molecules within living cells as method, described below). The majority of measured SRP well as molecules that are liberated into the environment comprises orthophosphate and other related derivatives after decay of an organism. The major source of terrestrial – 2– (e.g., H2PO4 ,HPO4 depending on pH) but other forms organic phosphorus is plant material, which is released as of phosphorus may also be included due to experimental vegetation undergoes decay; however, microbial and ani- inaccuracy. Therefore, although SRP tends to closely reflect mal sources also contribute significantly. In the marine the amount of orthophosphate in a sample, the values may environment, organic phosphorus comes from a variety of not be identical. sources (e.g., plankton, fish excrement, advection from The most common assay for measuring SRP is the land), the relative contributions of which differ widely ascorbic acid method, which is approved by the US depending on location in the ocean. In contrast to organic Environmental Protection Agency for monitoring phos- forms, inorganic phosphorus compounds are not always phate in environmental samples. In this method, ascorbic directly of biogenic origin. Rather, they also encompass acid and ammonium molybdate react with SRP in the phosphorus derived from the weathering of phosphate- sample, forming a blue compound that can be observed containing minerals, including dissolved and particulate visually or determined spectrophotometrically. Assays for orthophosphate. measuring total phosphorus are also based on the ascorbic acid method, but begin with a step to transform all of the phosphorus in the sample to orthophosphate (typically Phosphorus Sources, Sinks, and Transport through digestion by heating the sample in the presence Pathways of acid). After digestion, the sample is analyzed by the ascorbic acid method. A filtration step is typically not The phosphorus cycle encompasses numerous living and included in either of these methods, and accordingly in nonliving environmental reservoirs and various transport such cases, all size fractions are measured. pathways. In tracing the movement of phosphorus in the When phosphorus is measured in water samples, dis- environment, the interplay between physical and biological tinguishing forms that are part of particulate matter from processes becomes apparent. In addition to acting as reser- those that are in solution is often useful. Phosphorus is voirs of phosphorus in the environment (as discussed in this therefore classified as ‘soluble’ or ‘insoluble’, a distinction section), microbes contribute to the transformation of based on the method used to measure the sample. Soluble phosphorus within other reservoirs such as in soil or aqua- phosphorus includes all forms of phosphorus that are tic environments (see ‘Microbially mediated processes’). distributed in solution and that pass through a filter with Within the Earth’s crust, the abundance of phosphorus a given pore size (typically 0.45 mm), whereas the insolu- is 0.10–0.12% (on a weight basis), with the majority of ble, or particulate, fraction is the amount retained on the phosphorus existing as inorganic phosphate minerals filter. Measurements of soluble phosphorus include and phosphorus-containing organic compounds. A phos- both the ‘dissolved’ and ‘colloidal’ fractions. Dissolved phate mineral is any mineral in which phosphate anion phosphorus includes all forms that have entered a groups form tetrahedral complexes in association with 3– solute to form a homogeneous solution. (For example, cations, although arsenate (AsO4 ) and vanadanate 3– orthophosphate that is not bound to a cation is considered (VO4 ) may also be substituted in the crystalline Environmental Microbiology and Ecology | Phosphorus Cycle 325 structure. Apatite is the most abundant group of phos- chloride, each being named for the anion that is most phate minerals, comprising hydroxyapatite, fluorapatite, abundant in the mineral. Phosphate minerals generally and chlorapatite (Table 1). These three forms of apatite form in the environment in magmatic processes or share nearly identical crystalline structures, but differ in through precipitation from solution (which may be their relative proportions of hydroxide, fluoride, and microbially mediated), and the chemical composition of the minerals depends on the ion or ions present in solu- Table 1 Phosphate minerals and their chemical tion at the time of precipitation. For this reason, it is not compositions. Apatite is the general term for the three uncommon for natural deposits of phosphate minerals to minerals hydroxylapatite, fluorapatite, and chlorapatite be heterogeneous, rather than composed of one homogeneous type of phosphate mineral. These natural deposits Apatite Ca5(PO4)3(F,Cl,OH) Hydroxylapatite Ca5(PO4)3OH of phosphate minerals are collectively called ‘phosphor- Fluorapatite Ca5(PO4)3F ites’ to reflect variations in their chemical compositions. Chlorapatite Ca5(PO4)3Cl Soils and lake sediments are another terrestrial reser- Frankolite Ca 10ab voir of phosphorus, comprising primarily inorganic NaaMgb(PO4)6x(CO3)xyz(CO3F)y(SO4)zF2 Lazulite (Mg,Fe)Al2(PO4)2(OH)2 phosphorus from weathered phosphate minerals, along Monazite (Ce,La,Y,Th)PO4 with organic phosphorus from the decomposition, excre- Pyromorphite Pb5(PO4)3Cl tion, and lysis of biota (Figure 1). The behavior of Strengite FePO4?2H2O phosphorus in soils largely depends on the particular Triphylite Li(Fe,Mn)PO 4 characteristics of each soil, and besides microbial activity, Turquoise CuAl6(PO4)4(OH)8?5H2O Variscite AlPO4?2H2O factors such as temperature, pH, and the degree of oxy- Vauxite FeAl2(PO4)2(OH)2?6H2O genation all influence phosphorus mobility. In soils, Vivianite Fe3(PO4)2?8H2O inorganic phosphorus is typically associated with Al, Wavellite Al (PO ) (OH) ?5H O 3 4 2 3 2 Ca, or Fe, and each compound has unique solubility

Aerosol dust transport

Terrestrial deposition

Erosion and over land flow Eolian Riverine input deposition Rock Weathering Desorption Mineral Primary production Grazing Sinking and Marine formation 3– burial PO biota Soil 4 Upwelling Terrestrial Sinking of Phytoplankton Senescence Microbes biota particulate Assimilation Fe-bound P Senescence Organic P Euphotic zone

Mineralization Sinking Deep ocean Weathering detritus Microbes Assimilation Assimilation PO 3– Abiotic weathering and 4 phosphogenesis Organic P Solubilization Microbial loop

Mineral Mineral P 3– Mineralization Sinking formation PO4 detritus Solubilization Burial Burial Minerial P Minerial Organic P formation Burial Figure 1 Schematic diagram of the phosphorus cycle showing phosphorus reservoirs (living in green boxes; nonliving in gray boxes), physical transport pathways (blue arrows), and microbially mediated transformations (green arrows). 326 Environmental Microbiology and Ecology | Phosphorus Cycle characteristics that determine the availability of phos- continental margins and estuaries, through immediate phate to plants. The mobility and bioavailability of sedimentation and biological assimilation. The remaining phosphate in soils are limited primarily by adsorption phosphorus enters the dynamic surface ocean, also called (the physical adherence or bonding of phosphate ions the euphotic zone, in which nearly all bioavailable phos- onto the surfaces of other molecules), and the rate of phorus is sequestered within biota through primary microbially mediated mineralization of organic forms of production. Upon death of the organisms, a fraction of phosphorus. Mineralization is discussed in detail in the the biologically sequestered phosphorus sinks below the section titled ‘Microbially mediated processes’. euphotic zone and most of it is regenerated into bio- Marine sediments also represent an important phos- available forms like orthophosphate by heterotrophic phorus reservoir, but because the physical and chemical organisms. This recycling is part of the so-called ‘micro- factors affecting marine sediment differ considerably from bial loop’. Physical processes such as upwelling and deep those on land, processes controlling phosphorus dynamics convective mixing draw the deep water, which, in most in marine sediments are somewhat different from that of parts of the ocean, is nutrient-rich compared to the sur- soils. In marine sediment, phosphate can be present in face waters in the euphotic zone, where up to 95% of it is insoluble inorganic phosphates minerals (such as phos- reused in primary production. The remainder is removed phorites), which are relatively immobile. Phosphate can from the ocean reservoir through particulate sedimenta- also be sorbed onto iron or manganese oxyhydroxides. tion, mineral formation (which may be microbially The sorbed phosphate can regain mobility in response to mediated), and scavenging by iron and manganese changes in the redox potential at the sediment–water oxyhydroxides, all of which deposit phosphorus as a interface and thus is considered more mobile. As in ter- component of ocean sediment. restrial sediments, phosphorus in marine detrital organic The phosphorus cycle differs from the cycles of other matter can also become remobilized as decomposition biologically important elements, such as carbon, nitrogen, progresses through microbially mediated processes. and sulfur, in that it lacks a significant gaseous compo- Biota (i.e., microbes, plants, and animals) serve as nent; nearly all phosphorus in the environment resides another reservoir of phosphorus in the environment, as either in solid or in aqueous forms. The one exception to they assimilate phosphorus within their cellular biomass. this rule is the volatile compound phosphine (PH3, also Biota can contribute significantly to environmental phos- called phosphane), a colorless, poisonous gas formed phorus levels; for example, microbial communities in the environment from the breakdown of alkali metal contribute 0.5–7.5% of total phosphorus in grassland and or alkali earth metal phosphides with water. This process pasture topsoil, and up to 26% in indigenous forests. is poorly characterized and likely comprises various Microbes are also responsible for generating the myriad multistage chemical reactions. Microbially mediated of organic phosphorus compounds found throughout the phosphine production can be a major source of the gas environment. In particular, microbes and primary produ- in engineered systems (e.g., sewage treatment facilities cers play an important role in providing nutrition, and constructed wastewater treatment wetlands) where including phosphorus, to higher trophic levels by making organic phosphorus is abundant and reducing conditions it biologically available (bioavailable). Phosphorus assim- are common, suggesting that microbes could also play a ilation is a microbially mediated process, which is role in phosphine formation in natural systems (although discussed in the section titled ‘Transitory immobilization’. the direct enzymatic production of phosphine has not yet Phosphorus is transported within the environment been identified). Although phosphorus can exist as phos- through various mass transfer pathways. For example, phine, the gas does not persist in the environment owing rivers are important in the phosphorus cycle as both to rapid autoxidation, precluding significant accumula- reservoirs and transport pathways. Phosphorus that has tion of phosphine in the atmosphere. Phosphine is weathered from minerals and has leached or eroded from therefore a minor component of the environmental phos- soils enters rivers through a variety of vectors, including phorus pool. dissolved and particulate forms in water from overland The absence of a significant gaseous phase does not flow and in groundwater, and particulates brought by eliminate the atmosphere as an important reservoir in the wind. Approximately 95% of phosphorus in rivers is phosphorus cycle. When weathering and erosion of soils particulate, and approximately 40% of that is bound generate inorganic and organic particulate phosphorus, within organic compounds. Rivers influence the distribu- wind transports some of the particles from their source tion of phosphorus in soils and lakes by contributing or to a new location. These particles can include mineral removing phosphorus, and riverine input is the single dust, pollen and plant debris, insect fragments, and largest source of phosphorus to the oceans. organic phosphorus bound to larger particles. This dis- A number of outcomes are possible for phosphorus tribution of terrestrial particulate phosphorus, termed entering the ocean. Much of the riverine phosphorus eolian deposition, plays an important role in delivering flux is trapped in near-shore areas of the ocean, such as nutrients to the oceans. In oligotrophic ocean waters Environmental Microbiology and Ecology | Phosphorus Cycle 327 where nutrient levels are naturally low, such as in the Production of organic and inorganic acids is the pri- open ocean gyres where riverine inputs do not extend and mary mechanism of microbial phosphorus solubilization. significant upwelling does not occur, eolian deposition In this process, biogenic acid interacts with phosphorus may comprise a large portion of the nutrient flux that is minerals to form mono- and dibasic phosphates, thereby available for primary production. The eolian phosphorus bringing phosphorus into solution. Chemoautotrophic flux to the oceans is approximately 1 1012 g year1,of bacteria (e.g., nitrifying bacteria and Thiobacillus spp.) which approximately half is organic and the other half is generate nitric and sulfuric acids by oxidizing ammonium inorganic. The solubility, and therefore bioavailability, of and sulfur, respectively, and these acids are able to liber- the phosphorus in eolian particulate matter differs signif- ate soluble phosphorus from apatite, the most abundant icantly depending on its source; however, estimates phosphorus mineral. Production of organic acids occurs in suggest that approximately 15–50% is typically soluble. numerous microbial taxa, and contributes to the solubilization of phosphorus minerals. In addition to acid production, microbially mediated redox reactions contribute to phosphorus solubilization Microbially Mediated Processes through the reduction of iron oxyhydroxides and associated ferric phosphate (strengite). In this process, dissimilatory Weathering iron reduction of ferric phosphates liberates soluble ferrous Rock material exposed to the atmosphere breaks down, or iron as well as orthophosphate associated with it. This weathers, as a result of numerous environmental pro- occurs under reducing conditions, such as in flooded, anoxic cesses. Weathering processes are classified into two soils and in some benthic aquatic environments. In another categories. In mechanical weathering, physical processes redox process, hydrogen sulfide (H2S) produced by sulfur- (including thermal expansion, pressure release, hydraulic reducing bacteria reduces the ferric iron in iron phosphate action, salt crystal formation, freeze–thaw, and frost (FePO4) to ferrous iron. In this reaction, iron sulfide and wedge events) cause deterioration of rock material with- elemental sulfur are precipitated, and orthophosphate is out changing the chemical composition of the parent generated. material. In contrast, chemical weathering causes dete- Microbes also produce chelating compounds that con- rioration by altering the chemical structure of the tribute to phosphorus mineral solubilization. Chelation is minerals that the rock is made of. Chemical weathering the reversible binding (complexation) of a ligand to a metal processes include dissolution, hydrolysis, hydration, and ion. Chelators increase the solubility of insoluble phosphate oxidation–reduction (redox) reactions. Biological organ- mineral salts by complexing the metal cations, thereby isms can contribute to mechanical weathering by altering making dissolution of the salt more energetically favorable. the microenvironments at the surface of the parent mate- Examples of common chelators produced by microbes rial (e.g., by increasing local humidity or by forming include citrate, oxalate, lactate, and 2-ketogluconate. biofilms on surfaces); however, most biological weathering processes are classified as chemical weathering because they chemically alter the composition of the Mineralization parent rock material directly or indirectly. These biological weathering processes are also referred to as Plant and animal detritus comprises a large reservoir of solubilization. organic phosphorus in the soil environment. However, because organically bound phosphorus sources are generally unable to cross cell membranes, most of the organic Solubilization phosphorus from the detrital pool is not directly available Inorganic phosphorus can occur in nature in soluble and to many living organisms. In order to become bioavail- insoluble forms. The solubility of the most abundant form able, phosphorus bound to organic material must first be of inorganic phosphorus, orthophosphate, is determined mineralized to phosphate. Mineralization is the process in by the ambient pH and the cation to which it is bound as a which organically bound phosphorus is converted to inor- mineral (e.g., Ca2þ,Mg2þ,Fe2þ,Fe3þ,andAl3þ). ganic phosphate, and is accomplished through the activity Microbially mediated phosphorus solubilization plays an of a suite of microbial enzymes. Because this process important role in the conversion of insoluble phosphorus makes available nutrients that would otherwise be seques- minerals into soluble forms of phosphorus. Solubilization tered in nonreactive forms, mineralization provides a vital directly benefits the microbes that perform it by provid- link between the detrital pool and living organisms. It is ing the bioavailable phosphorus needed for growth. estimated that approximately 70–80% of soil microbes Similarly, the process benefits other organisms (including are able to participate in phosphorus mineralization. other cells, fungi, and higher plants) that are able to utilize In general, mineralization is optimal and more phos- the surplus of solubilized phosphorus. phorus is liberated in uncultivated soils than in soils 328 Environmental Microbiology and Ecology | Phosphorus Cycle undergoing extensive cultivation, and a higher proportion to simply as phosphatases in the scientific literature, rather of the organic phosphorus pool is mineralized in unculti- than by their full name, and context is often necessary to vated soils. Further, mineralization rates tend to be higher determine which group is being referenced. Therefore, a in soils where inorganic phosphates are actively taken up phosphomonoesterase with a pH optima near 8 might be and sequestered in plants and where microbial grazers are referred to as an ‘alkaline phosphatase’ rather than an present, as would be expected in mature, uncultivated ‘alkaline phosphomonoesterase’ (PhoA) in the scientific soils with fully developed, autochthonous microbial com- literature. munities and trophic structures. As in many enzyme- A similar class of enzymes, phosphodiesterases, attack catalyzed systems, mineralization is encouraged by higher diester bonds in which a phosphate group is bonded to levels of available substrate; however, high levels of two separate carbon atoms, such as in phospholipids and inorganic phosphate (the product) do not impede the nucleic acids. For example, the sugar-phosphate back- reaction, and mineralization will occur even if an abun- bone in DNA comprises phosphodiester bonds. With dance of phosphate is present. Other ambient conditions water added across the phosphorus–carbon bond, cleaving favoring phosphorus mineralization include warm soil of a diester proceeds similarly to the monoester reaction, temperatures and near-neutral pH values, which are con- yielding phosphate and an alcohol. Once a diester has ditions that also favor mineralization of other elements. undergone hydrolysis, the resulting alcohol phosphomo- Accordingly, phosphorus mineralization rates tend to noester must undergo another hydrolysis step, catalyzed reflect rates of ammonification and carbon mineralization by a phosphomonoesterase, for phosphorus mineraliza- in soils, and together these microbially mediated miner- tion to be complete. alization processes yield a C:N:P ratio that is similar to the Nucleic acids represent an important source of organic ratio of these elements in humus (i.e., the organic soil nutrients and are released from a cell upon lysis. Their fraction consisting of decomposed vegetable or animal rapid degradation and relatively low concentrations in the matter.) environment suggest an important role for nucleic acids Enzymesinvolvedinmineralizationcompriseadiverse as microbial nutrient sources. Many heterotrophic group of proteins, called phosphatases, with a broad range of microbes are able to use nucleic acids as their only source substrates and substrate affinities, and varying conditions for of phosphorus, nitrogen, and carbon, and numerous others optimal activity. In addition, phosphatases can either be can use nucleic acids to supplement their nutritional constitutively expressed by an organism, or the expression requirements. The mineralization of phosphorus from can be upregulated under conditions of low phosphate (and nucleic acids proceeds in a two-step process involving in some cases, low carbon). Enzyme synthesis allows micro- two different enzymes. In the first step, depolymerizing bial cells to access organic phosphorus during periods of nuclease enzymes such as DNase for DNA and RNase phosphate limitation, thereby avoiding the growth limitation for RNA cleave the nucleic acid molecules into their and physical stress associated with nutrient deprivation. constituent monomer nucleotides. Complete phosphorus Phosphatasescanbeclassifiedbasedonthetypeofcarbon– mineralization of the resulting fragments proceeds via the phosphorus bond they cleave, but any given phosphatase activity of nucleotidase enzymes, which yield a phosphate enzyme may catalyze reactions for numerous organic phos- group and a nucleoside molecule after hydrolysis. phorus compounds. In other words, a phosphatase enzyme Phytins, which are complex organic molecules con- has specific substrate requirements for a class of compounds, taining up to six phosphate groups, are mineralized by a but lacks specificity in selecting substrates from within that class of enzymes called phytases. Phytases catalyze class. The most common categories of microbial phospha- hydrolysis of the phosphate ester bonds that attach phos- tases contributing to phosphorus mineralization include phate groups to the inositol ring, yielding reactive phosphomonoesterases, phosphodiesterases, nucleases, and phosphate and a series of lower phosphoric esters. The nucleotidases, as well as phytases. location on the ring of the first hydrolysis reaction Phosphomonoesterases catalyze reactions with phos- catalyzed by a phytase determines its classification; phomonoesters, which are compounds in which one 3-phytases initiate hydrolysis at the phosphate ester phosphate group is covalently bound to one carbon atom. bond of the ring’s third carbon atom, whereas 6-phytases The reaction involves the hydrolysis of the phosphorus– initiate at the sixth carbon atom. Hydrolysis by 6-phytases carbon bond, generating a free phosphate molecule and an always leads to complete dephosphorylation of the inosi- alcohol as products. One example of a phosphomonoester tol ring, whereas the 3-phytases may lead to incomplete is glycerol phosphate, a source of phosphate and carbon dephosphorylation. Phytases are produced broadly by for some microbes. Phosphomonoesterases are further microbes, plants, and animals. In general, plants produce classified as ‘acid’ or ‘alkaline’ on the basis of their optimal 6-phytases and microbes produce 3-phytases; however, pH ranges for maximum catalytic activity. Probably as a 6-phytase activity has been observed in Escherichia coli. result of their ubiquity and importance in phosphorus Microbial phytase activity is optimal over a broader range mineralization, phosphomonoesterases tend to be referred of pH values as compared to plant phytases, with pH Environmental Microbiology and Ecology | Phosphorus Cycle 329 optima spanning from 2 to 6 (plant phytases are optimal the hydrolytic products of glycerol phosphate and other near pH 5). In addition to being affected by ambient pH, bioenergetically important molecules has also been used hydrolysis by phytases is also influenced by the degree of to estimate phosphatase activity in bulk populations. complexation of the phytin substrate with metal cations. A major drawback to measuring bulk phosphatase Because many phosphatase enzymes are synthesized in activity is that it provides limited information, if any, response to low environmental phosphate levels (i.e., when about which members of the microbial community the cells experience phosphate limitation), phosphatase experience phosphate limitation at the time of sampling. activity has been used extensively as a metric for determin- This can be addressed to some extent by size-fractionat- ing the nutrient status of microbial communities. The ing cells (as on a filter) before incubation with the activity of phosphatase enzymes has been measured in substrate, thereby allowing phosphatase activity to be many terrestrial, limnic, and marine environments using a assigned to gross taxonomic classes of organisms. variety of methods, and numerous laboratory studies have However, size fractionation introduces other obstacles also been conducted. In the environment, the bulk phos- for data interpretation, and results must be interpreted phatase activity of an entire microbial community is with care. For example, activity in different size fractions commonly measured by incubating soil, sediment, or can be skewed by groups of bacteria that coalesce to form water samples with a phosphate-bound substrate in which larger particles, although the individual cells are small the hydrolytic product undergoes a color change that can and would otherwise be grouped with smaller size frac- be observed visually or spectrophotometrically, such as tions. Studies with mixed populations of bacteria and para-nitrophenyl phosphate (PNP) (Figures 2(a)and green algae showed that 44% of the measured phospha- 2(b)), phenolphthalein phosphate, glycerophosphate, and tase activity was attributable to aggregated groups of cells. 5-bromo-4-chloro-3-indolyl-phosphate (Figure 2(c)). Moreover, in the marine environment, substantial phos- In addition, measurements can be made fluorometrically phatase activity has been shown to persist for 3–6 weeks at for the substrates 3-O-methylfluoresein phosphate and 50% of initial levels in water samples filtered to remove 4-methylumbellyferyl phosphate. Radiometric analyses particles. These observations suggest that phosphatases can similarly be made using 32P-labeled glycerol phos- free in solution or bound to soluble organic material can phate (or an equivalent molecule). Chemical analysis of contribute a significant amount of phosphatase activity,

(a) (b)

PNP Relative absorptionRelative 200 400 600 Wavelength (nm) (c) +P –P

psr1-1 psr1-2 psr 2

psr1-2 psr 2

Figure 2 (a) The para-nitrophenyl phosphate (PNP) assay for alkaline phosphatase activity produces a yellow color in the presence of the enzyme. (b) The PNP assay quantifies alkaline phosphatase activity based on the absorption of light at 380 nm. (c) The 5 bromo-4- chloro-3-indolyl-phosphate assay with Chlamydomonas algae under phosphate-replete (left panel) and phosphate-limited (middle panel) conditions shows phosphatase activity using the blue coloration formed around the cells when they express the enzyme. Key (right panel) identifies mutants used in the study (wt is wild type). The phosphatase of the wild-type cells is induced in phosphate-free medium. Reproduced from Shimogawara K, Wykoff DD, Usuda H, and Grossman AR (1999). Chlamydomonas reinhardtii mutants abnormal in their responses to phosphorus deprivation. Plant Physiology 120: 685–693, with permission from the American Society of Plant Biologists. 330 Environmental Microbiology and Ecology | Phosphorus Cycle potentially leading to overestimates of phosphatase activ- Immobilization ity in the small cell size fraction. A difficulty common to Immobilization refers to the process by which labile both bulk- and size-fractionated samples is that phospha- phosphorus is sequestered and removed from the envir- tases can persist for long periods of time without being onmental reservoir of reactive phosphorus for a period of bound to a living cell. It is not uncommon for microbial time. Immobilization processes can generally be grouped cells to retain phosphatase activity for months or years into two categories. The first category, transitory immo- after being dried or preserved, indicating that cell viabi- bilization or cellular assimilation, includes all processes lity is not critical for maintaining phosphatase enzymes that sequester phosphorus within living microbial cells over these time periods, and dead cells may contribute to and is rapidly reversible upon cell death. The second the overall phosphatase activity in a sample. category, mineral formation, encompasses processes that Several methods have been developed to overcome the generate phosphorus-containing minerals. limitations of bulk measurements by directly labeling cells when phosphatases are present. These methods allow phosphatase activity to be attributed to individual Transitory immobilization cells or taxa, allowing greater resolution of the phosphate Transitory immobilization, or assimilation, is an impor- status of organisms within a mixed community. Direct tant mechanism of phosphorus sequestration in soil and cell staining with azo dyes or precipitation of lead freshwater environments. Within cells, phosphorus is phosphate at the site of enzyme-mediated phosphate incorporated in numerous essential biological molecules release has been used together with light microscopy to and is required in larger quantities than many other ele- visualize phosphatase activity on individual cells. ments. However, unlike other biologically important Similarly, enzyme-labeled fluorescence (ELF) labels nutrients such as nitrogen and sulfur that must first individual cells with a fluorescent precipitate (ELF-97) undergo reduction before being incorporated into the after hydrolysis of the nonfluorescent substrate molecule cell, phosphorus remains oxidized before and after assim- (2-(59-chloro-29phosphoryloxyphenyl)-6-chloro-4-(3H)- ilation. Because mineralization of cellular material occurs quinazolinone) at the site of the enzyme (Figures 2(c) rapidly after cell death, cellular assimilation of and 3). phosphorus into biological macromolecules leads to

(a) (b)

10 µm 30 µm (c) (d)

4 µm 5 µm

Figure 3 Micrographs of ELF-97-labeled phytoplankton from the euphotic zone in the Gulf of Aqaba (a) Trichodesmium sp., (b) Ceratium sp., (c) coccolithophore, and (d) Cyanothece sp. For each pair, the left panel is a view under visible light and the right panel under UV illumination. ELF-97-labeled areas appear as bright areas under UV illumination and show the location of phosphatase enzymes on the cells. Reproduced from Mackey KRM, Labiosa RG, Calhoun M, Street JH, Post AF, and Paytan A (2007). Phosphorus availability, phytoplankton community dynamics, and taxon-specific phosphorus status in the Gulf of Aqaba, Red Sea. Limnology and Oceanography 52: 873–885, with permission from the American Society of Limnology and Oceanography, Inc. Environmental Microbiology and Ecology | Phosphorus Cycle 331 relatively short-term phosphorus retention in living cells (e.g., Zn2þ,Fe2þ,Mn2þ,Fe3þ,Ca2þ,Mg2þ), as well as where the duration is related to the characteristics of the proteins and starches within mature seeds and when pre- microbial community in question. Within the cellular sent in the environment. The complexed form of phytic reservoir, phosphorus is present as different compounds acid, also known as phytin, can be a persistent phosphorus and serves various functions. reservoir in the environment because it is less accessible Phospholipids are lipids in which a phosphate group to degradation by hydrolytic enzymes when complexed. has replaced one of the fatty acid groups. Lipids are In addition to biological molecules such as nucleic acids generally hydrophobic; however, phospholipids are and phospholipids, which by weight consist primarily amphipathic, meaning that each molecule has a hyrdro- of carbon along with smaller portions of phosphorus, the philic portion and a hydrophobic portion. The phosphate intracellular accumulation of polyphosphate granules group is responsible for giving phospholipids their par- in microbial cells is an important type of transitory phos- tially hydrophilic character, hence imparting a wide range phorus immobilization. Polyphosphates are chains of of biochemical properties. In the cell, phospholipids are 3–1000 phosphate residues connected by anhydride bonds important in the formation of biological membranes and that form by the activity of polyphosphate kinase enzymes, in some signal transduction pathways. and therefore represent a highly concentrated reservoir of Nucleotides are biological compounds consisting of a phosphorus in the cell. The energy stored in the anhydride pentose sugar, a purine or pyrimidine base, and one or bonds can be used by the microbial cell during periods of more phosphate groups. Nucleotides are the structural starvation. Polyphosphates may also serve as ligands for subunits (monomers) of RNA and DNA, and alternating metal cations such as calcium, aluminum, and manganese bonds between the sugar and phosphate groups form the in some microbes; however, the extent and the elemental backbones of these nucleic acids. Specifically, the phos- stoichiometry of intracellular polyphosphate cation com- phate groups form phosphodiester bonds between the plexation vary among organisms. third and fifth carbon atoms of adjacent sugar rings, Phosphorus immobilized within cells is considered hence imparting directionality to the molecule. In addi- transitory because it is able to rapidly reenter the reactive tion, nucleotides are present as several major cofactors in phosphate pool after cell death through microbially the cell (e.g., flavin adenine dinucleotide, nicotinamide mediated mineralization processes. The immobilization adenine dinucleotide phosphate) that have important of phosphorus via cellular assimilation is therefore rela- functions in cell signaling and metabolism. tively brief (i.e., within the lifetime of a cell) compared Adenosine triphosphate (ATP) is a nucleotide that with other processes within the phosphorus cycle, some of performs multiple functions of considerable importance which occur over geological timescales. to the cell. The primary function of ATP is to aid in intracellular energy transfer by storing energy that is Phosphate mineral formation generated during photosynthesis and respiration so that Phosphate mineral formation represents another phos- it can be used in other cellular processes that require phorus sink that is influenced by microbial activity; energy (e.g., cell division and biosynthetic reactions). In however, it encompasses processes other than cellular assim- the cell, phosphate can be assimilated in ATP through ilation and short-term storage of phosphorus as biological substrate-level phosphorylation, oxidative phosphoryla- molecules. In mineral formation (also called phosphogen- tion, photophosphorylation, and via the adenylate kinase esis), phosphate anions react with cations in the environment reaction. ATP is also active in signal transduction path- to form insoluble precipitates. Sediments that comprise sig- ways, where it can be used as a substrate for kinase nificant amounts of phosphorus-containing minerals are enzymes in reactions that transfer phosphate groups to called ‘phosphorites’, and may contain apatite, francolite, proteins and lipids, forming phosphoproteins and phos- and a number of other phosphorus minerals (Table 1). pholipids, respectively. Phosphorylation is an important Mineral formation is generally an important mechanism of and ubiquitous form of signal transduction in many phosphorus sequestration in marine environments where organisms. the high seawater calcium levels facilitate microbially Phytic acid (also called inositol hexaphosphate, IP6, mediated formation of insoluble phosphorites. The seques- phytate, and myoinositol 1,2,3,4,5,6-hexakis dihydrogen tration of phosphorus by this process retains (immobilizes) phosphate) is an organic, phosphorylated, cyclic, sugar phosphorus for longer periods of time than does transitory alcohol produced by plants and found in high concentra- immobilization. tions in seeds, and may also be produced by microbes. In For an insoluble mineral to form, the concentration of its fully phosphorylated form, six phosphate groups attach the ions forming the mineral must be high enough such to the inositol ring; however, various isomers of the less that supersaturation is reached and equilibrium of the highly substituted inositol phosphate molecules also precipitation reaction is shifted toward the product. In exist. Phytic acid is a highly reactive compound that addition, the physical and chemical characteristics of the forms stable complexes with a variety of mineral cations environment must be conducive to precipitation of that 332 Environmental Microbiology and Ecology | Phosphorus Cycle mineral based on its solubility characteristics, and factors within cells may also lead to phosphorus immobilization such as pH, redox state, and concentrations of co-occur- via mineral formation if phosphorus minerals are gener- ring ions all influence mineral precipitation. The mineral ated and stored within the cell. Intracellular formation of must also be stable in the environment for mineral for- mineral apatite is an example of phosphorus immobiliza- mation to constitute a long-term sink for phosphorus. tion that has been observed in some microbes (e.g., E. coli, Mineral formation occurs both authigenically and Bacterionema matruchotii) after incubation with calcium diagenetically in the environment. Authigenic mineral phosphate at a slightly basic pH. This process occurs in formation is the formation of insoluble precipitates living and dead cells, suggesting that the locally elevated (minerals) in situ rather than by having been transported reactive phosphate concentrations within the cell help or deposited in a location through secondary processes. In initiate apatite formation. Similarly, the formation of car- contrast, diagenetic mineral formation is the alteration of bonate fluorapatite after cell death has been observed in existing minerals by chemical changes occurring after the Gram-negative rods, possibly pseudomonads, in coastal initial deposition of a mineral (i.e., during or after burial marine sediment, and is believed to be an important and lithification). The primary type of diagenetic phos- phosphorite formation process in locations where sedi- phorus mineral formation in marine environments is the mentation rates are low. substitution of phosphate into calcium carbonate minerals such as calcite or aragonite. Microbes contribute to this process by mineralizing organic phosphorus to reactive Genetic Regulation of Microbially phosphate, which then substitutes diagenetically into cal- Mediated Processes cium carbonate. In authigenic mineral formation, microbes may gener- Microbially mediated processes, including those involved ate reactive phosphate from the mineralization of organic in the phosphorus cycle, are the outcome of numerous phosphorus sources, and the resulting localized high phos- biological pathways occurring in concert across diverse phate concentrations favor precipitation of phosphate microbial communities. Even cursory observations of nat- minerals. In soils, microbes convert organic phosphorus ural microbial communities demonstrate that while into phosphate, increasing its concentration in the soil microbially mediated processes influence and change the and promoting formation of stable minerals such as apatite. environment, the environment likewise shapes the activity In productive areas of the ocean, microbial mineralization of microbes, in many cases by providing feedback that of detrital matter at the sediment–water interface generates either inhibits or enhances the processes. (An example of reactive phosphate, some of which reacts with seawater this type of feedback is the synthesis of phosphomonoester- calcium to form phosphorite. (Reactive phosphate that ase enzymes, many of which are only present during does not contribute to mineral formation is available for periods of orthophosphate deprivation but not when ortho- biological assimilation by benthic microbes, or may be phosphate is abundant in the environment.) Similarly, reintroduced to the euphotic zone by diffusion and upwel- microbially mediated processes can also be controlled ling for use by phytoplankton.) indirectly by secondary factors (other than phosphorus) The accumulation of phosphorus in microbial cells that influence growth and metabolism, such as the during transitory immobilization also contributes to availability of oxidized nitrogen or sulfur in some chemoau- mineral formation by increasing the pool of phosphate totrophic microbes. that could react with cations to form minerals. This is These processes, which are manifest in the environ- particularly important in anoxic areas of the ocean and ment as the combined outcome of activities from a diverse soils where reactive phosphorus levels are low. Under microbial community, are in fact a result of genetic med- oxic conditions where reactive phosphate is more abun- iation within single cells. The regulation of genes in dant, luxury uptake and storage of phosphate as response to environmental stimuli determines how a cell polyphosphate molecules occur in some microbes (e.g., will respond to its environment, including if and how it Pseudomonas spp., Actinobacter spp.), as discussed above. will contribute to microbially mediated processes in Cells use the energy stored in polyphosphates to activate the phosphorus cycle. To understand gene regulation in an alternative organic electron acceptor when conditions greater detail, highly sensitive genetic and molecular shift toward anoxia, freeing substantial levels of reactive methods have been developed. Under laboratory condi- orthophosphate in the process. The sequestration and tions, these methods have elucidated pathways important release of phosphate by the cell under oxic and anoxic in the immobilization (i.e., phosphorus assimilation conditions, respectively, represent a mechanism by which into cell biomass) and mineralization (i.e., phosphatase microbes contribute to mineral formation because it gen- production) of phosphorus, as well as countless other erates locally elevated reactive phosphate concentrations pathways and processes. in the vicinity of the cells that are high enough to induce In E. coli, two major phosphate assimilation pathways precipitation of minerals. Accumulation of phosphate have been identified. The phosphate transport system Environmental Microbiology and Ecology | Phosphorus Cycle 333

(Pit), which comprises a hydrogen phosphate symport particular, the alkaline phosphomonoesterase gene powered by protonmotive force, is expressed constitu- (phoA) and homologues have been identified in numerous tively and provides the cell with sufficient phosphorus microbial taxa, and although the primary function of the for growth when phosphate concentrations in the media protein remains the same, factors that influence its are not limiting. When media phosphate concentrations expression and activity vary from organism to organism. decrease below a threshold concentration, the high-affi- The diversity of organisms and environmental conditions nity phosphate-specific transport (Pst) system becomes in which this gene exists allow microbially mediated engaged. This system has a 100-fold greater affinity for mineralization of phosphorus to occur in nearly every phosphate than Pit, enabling the cell to acquire phosphate environment where microbes are found. For example, from a limited reservoir. Uptake of phosphate through Pst photosynthetic cyanobacteria in the genus Synechococcus, is an ATP-dependent process (e.g., requires energy input which populate freshwater environments, coastal waters, from the cell). and vast areas of the open ocean, have the phoA gene along Pst is activated as part of the Pho regulon, a group of with many of the other genes encoded in the Pho regulon, operons that is expressed when phosphate levels are low. highlighting the global ubiquity of microbially mediated Activation of the Pho regulon is initiated through phos- processes in the phosphorus cycle. phorylation of the PhoB cytoplasmic protein, which, in its phosphorylated state, is a transcriptional activator of the operons within the Pho regulon. In addition to Pst, the Pho regulon also includes genes encoding PhoA, outer- Anthropogenic Alteration of the P Cycle: membrane porin proteins that facilitate diffusion of Eutrophication in Aquatic Ecosystems phosphate into the periplasm (PhoE), and proteins for the uptake and processing of glycerol-3-phosphate (ugp As discussed above, microbes have an important role operon) and phosphonates (phn operon). in nearly every aspect of the phosphorus cycle, and their Metabolism of glycerol-3-phosphate is an interesting activities help control the relative rates at which phosphorus strategy for heterotrophic microbes, such as E. coli, is mobilized and immobilized within the environment. because it is a potential source of both phosphate and However, humans also influence the phosphorus cycle and carbon for the cell. However, when grown under phos- alter the structure of microbial communities, causing devas- phate-deplete conditions and expressing ugp genes, cells tating ecological consequences. are only able to use glycerol-3-phosphate as a phosphate Postindustrial human activities, including deforesta- source, not as a carbon source. For cells to grow with tion, phosphorus mining, and agricultural practices, glycerol-3-phosphate as the only phosphate source, affect the phosphorus cycle by increasing the mobility of another carbon source must also be provided. The ugp phosphorus in the environment and causing it to accu- system is less efficient when internal cell phosphate levels mulate in soils and aquatic environments. Several factors are high, and is no longer expressed if external phosphate contribute to the mobilization of phosphorus by these levels increase above a threshold level. Another system activities. Deforestation and mining expose phosphate that is not part of the Pho regulon, the glp transport (and other) minerals in rock and soil to the atmosphere, system, is regulated by external and internal glycerol-3- leading to increased rates of weathering and erosion. phosphate levels rather than by phosphate concentrations. Agricultural soils are also highly susceptible to erosion, Unlike in the ugp system, glycerol-3-phosphate acquired making the localized elevation of phosphorus levels from by the glp system is able to serve as the sole source of application of fertilizers a particularly large source of the carbon and phosphate for the cell. Both ugp and glp anthropogenic phosphorus flux. As a result of these prac- systems facilitate the direct cellular uptake of glycerol- tices, recent estimates suggest that the net storage of 3-phosphate; however, each is regulated by different phosphorus in terrestrial and freshwater habitats has internal and external cues (i.e., phosphate or glycerol-3- increased 75% over preindustrial levels, and the total phosphate levels), and has a different nutritional strategy reactive phosphorus flux to the ocean is twofold higher (i.e., supplying phosphate alone vs. phosphate and carbon than prehuman levels. Consequently, eutrophication (the together). excessive growth of phytoplankton in response to over- These two systems are an example of how microbes, enrichment of a growth-limiting nutrient) has become a by developing multiple interrelated pathways, are able to widespread problem in lakes and estuaries throughout the contribute to microbially mediated processes in the phos- world, carrying serious environmental, economic, esthetic, phorus cycle under a range of environmental and and human health consequences. Eutrophication has been physiological conditions Experimental evidence shows observed in many ecosystems, including freshwater lakes that the phosphate assimilation pathways in other hetero- such as Lake Erie, large estuaries such as the Chesapeake trophic bacteria are similar to E. coli, and many microbes Bay, and coastal areas such as the hypoxic ‘dead zone’ of are known to have portions of the Pho regulon. In the Gulf of Mexico. 334 Environmental Microbiology and Ecology | Phosphorus Cycle

Organic fertilizers (e.g., poultry litter, manure) are environments, and to contribute to the phosphorus cycle typically applied to crops based on the rate of crop under numerous and diverse environmental conditions. nitrogen uptake, resulting in the overapplication of phos- Human alteration of the natural phosphorus cycle causes phorous and its rapid accumulation in soils. Elevated soil unintended consequences in microbial communities, and phosphorus levels increase the amount of phosphorus in serious environmental, economic, esthetic, and human runoff and ultimately lead to the accumulation of phos- health problems are caused by microbial responses to the phorus in lakes and estuaries. When phosphorus from anthropogenic introduction of excess phosphorus to sen- agriculture application is washed into water bodies sitive aquatic ecosystems. where phosphorus limits production, substantial changes in the microbial community occur. Reversal of phosphorus limitation leads to the rapid growth of bloom- See also: Algal Blooms; Ecology, Microbial; Freshwater forming phytoplankton, some of which are toxic or Habitats; Marine Habitats; Sediment Habitats, including nuisance species (such as Pfiesteria sp.) that are harmful Watery to aquatic organisms and humans. As the bloom exhausts the supply of phosphorus, the phytoplankton senesce, sink to the bottom of the water body, and are decomposed by Further Reading the heterotrophic microbial community. At depth, where Alexander M (1967) Microbial transformations of phosphorus. In: light levels are low, photosynthetic phytoplankton are not Introduction to Soil Microbiology, 2nd edn. New York, NY: John able to balance the metabolic oxygen demands of the Wiley and Sons. heterotrophs, and anoxia occurs in the bottom waters. Compton J, Mallinson CR, Glenn D, et al. (2000) Variations in the global phosphorus cycle. In: Glennal CR, et al. (eds.) Marine Authigenesis: Anoxia damages the benthic environment, leading to From Global to Microbial Tulsa: Special Publication 66. SEPM fish kills and harming benthic invertebrate communities. (Society for Sedimentary Geology). Loss of submerged aquatic vegetation, coral reef death, Dyhrman ST, Ammerman JW, and Van Mooy BAS (2007) Microbes and the marine phosphorus cycle. Oceanography 20: 110–116. human shellfish poisoning, and a reduction in biodiversity Ehrlich HL (1999) Microbes as geologic agents: Their role in mineral are among the possible outcomes caused by microbial formation. Geomicrobiology Journal 16: 135–153. responses to the anthropogenic introduction of excess Ehrlich HL (2002) Geomicrobial interactions with phosphorus. In: Geomicrobiology, 4th edn. New York, NY: CRC Press, Inc. phosphorus to sensitive aquatic ecosystems. Follmi KB (1996) The phosphorus cycle, phosphogenesis and marine phosphate-rich deposits. Earth-Science Reviews 40: 55–124. Heath RT (2005) Microbial turnover of organic phosphorus in aquatic systems. In: Turner BL, Frossard E, and Baldwin DS (eds.) Organic Conclusion Phosphorus in the Environment. Cambridge, MA: CABI Publishing. Oberson A and Joner EJ (2005) Microbial turnover of phosphorus in soil. Microbially mediated processes in the phosphorus cycle In: Turner BL, Frossard E, and Baldwin DS (eds.) Organic Phosphorus in the Environment. Cambridge, MA: CABI Publishing. forge a critical link between the geosphere and biosphere Paytan A and McLaughlin K (2007) The oceanic phosphorus cycle. by assimilating phosphorus within biological molecules Chemical Reviews 107: 563–576. and contributing to chemical transformations of phos- Ruttenberg KC (2003) The global phosphorus cycle. In: William H Schlesinger (ed.), Heinrich D Holland and Karl K. Turekian (Executive phorus in the environment. In addition to acting as living eds.) Treatise on Geochemistry, vol. 8, pp. 585–643, 682. Elsevier. reservoirs of phosphorus, microbes also contribute to the Sharpley AN, Daniel T, Sims T, et al. (2003) Agricultural Phosphorus and transformation of phosphorus within other nonliving Eutrophication, 2nd edn, p. 149. U.S. Department of Agriculture, Agricultural Research Service, ARS. reservoirs, such as rock, soils, rivers, lakes, and oceans. Stewart JWB and Tiessen H (1987) Dynamics of soil organic Microbially mediated phosphorus transformation phosphorus. Biogeochemistry 4: 41–60. includes processes that increase the bioavailability of Sundby B, Gobeil C, Silverberg N, et al. (1992) The phosphorus cycle in coastal marine sediments. Limnology and Oceanography phosphorus in the environment, such as weathering, solu- 37: 1129–1145. bilization, and mineralization, as well as those that USEPA (1983) Methods for Chemical Analysis of Water and Wastes. decrease its bioavailability, such as assimilation and 2nd edn. Washington, DC: Environmental Protection Agency. USEPA (1996) Environmental Indicators of Water Quality in the United mineral formation. These large-scale environmental pro- States. Washington, DC: Environmental Protection Agency. cesses are the outcome of numerous biological pathways Whitton BA, Al-Shehri AM, Ellwood NTW, et al. (2005) Ecological occurring in concert across diverse microbial commu- aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. In: Turner BL, Frossard E, and Baldwin DS (eds.) nities. Genetic diversity and finely tuned regulation of Organic Phosphorus in the Environment, Cambridge, MA: CABI gene expression allow microbes to adapt to harsh Publishing.