International Journal of Recycling Organic Waste in Agriculture (IJROWA)

https://dx.doi.org/10.57647/ijrowa-ybbx-kp03

A comprehensive review on organic waste compost as an effective phosphorus source for sustainable agriculture

Lady Johanna Boho´rquez-Sandoval1

, Jose´ Francisco Garc´ıa-Molano2,∗

, Jose´ Antonio Pascual-Valero3

, Margarita Ros-Mun˜oz3

1University of Murcia, International Doctoral School, University Campus of Espinardo, Murcia, Spain.

2Juan de Castellanos University Foundation, Department of Agricultural and Environmental Sciences Tunja, Colombia.

3CSIC-CEBAS. Department of Soil and Water Conservation, University Campus of Espinardo, Murcia, Spain.

∗Corresponding author: [email protected]

Review Paper

Received:

05 October 2023 Revised:

13 Februrary 2024 Accepted:

20 June 2024 Published online: 07 August 2024

Abstract:

Purpose: The transformation of Organic Waste through composting has become a source of organic matter that, through microbial action, generates molecules conducive to phosphate solubilization and produces fractions of Po and Pi readily available for plants. For this reason, this review focused on analyzing various research studies where Organic Waste is utilized to release available phosphorus and thus improve agricultural production.

Method: One hundred and eighteen articles were analyzed and synthesized from recognized databases, addressing the following topics: Phosphorus in the Earth’s crust, phosphorus recovery from Organic Waste, compost, metabolic pathways for phosphorus release in compost, and microbial activity for phosphorus release in compost.

Results: The selection of organic materials and the incorporation of MSP during the composting process favor the availability of P for plants. The compost microbiota associated with phosphorus not only enhances its availability but also may promote plant growth. Various mechanisms exist for P release, such as the enzymes β -1,4-glucosidase and β -D-fructofuranosidase, along with mycorrhizae facilitating P transport, the enzymatic cofactor pyrroloquinoline quinone, and the function of phosphorus genes contributing to its availability, thereby promoting sustainable agricultural practices.

Conclusion: Composts can serve as valuable P sources for plants, wherein their existing microbiota enhances phosphorus availability, facilitating increased phosphorus recycling through symbiotic relationships, microbial interactions, and the action of phosphorus genes, thereby ensuring sustainable agriculture.

Keywords: Enzymatic activity; Organic acids; Organic waste; Phytohormones; Phosphate solubilizers

‌Introduction

Phosphorus plays a vital role in various physiological func- tions in plants, such as cell division, root development, and photosynthesis, as it is a component of essential molecules like phospholipids, nucleic acids, and ATP (Ortega, 2020). However, despite the assistance of specialized microorgan- isms in releasing phosphorus from compounds, it remains relatively scarce in the soil for plants (Atoloye et al., 2021). Phosphorus (P) is the eleventh most abundant element in the Earth’s crust (Corbridge, 2013), with a gross abundance ranging from 0.10% to 0.12% (w/w) (Fuller, 1972; Cor-
bridge, 2013). Therefore, total mineral phosphorus con- centrations in soil range from 35 to 5300 mg P/Kg, with an average of approximately 800 mgP/Kg to 1400 mgP/kg (Bowen, 1979; Azam et al., 2019; Walton et al., 2023). Mineral phosphorus in soil originates from igneous and sedimentary rocks, which are initially insoluble and must be solubilized for plant assimilation (Contrato, 2018). This input has been excessive over the years through highly soluble phosphates, and the unused remnants accumulate in the soil, either through multivalent metal chelation or clay and organic matter absorption, requiring application in each crop cycle. High concentrations of phosphate can

be found bound to other elements such as Ca, F, or Cl, forming apatite and fluorapatite, (Ca5(PO4)3F), chlorap- atite (Ca5(PO4)3Cl), and hydroxyapatite (Ca5(PO4)3OH) (Espinel, 2020). Other mineral sources of P in- clude lazulite ((Mg-Fe), Al2(PO4)2(OH)2), strengite (FePO4.2H2O), vauxite (FeAl2(PO4)2(OH)2.6H2O), vivian- ite (Fe3(PO4)2.8H2O), and variscite (AlPO4.2H2O) (Veith and Sposito, 1977).
Approximately 30% to 65% of total soil phosphorus exists in organic forms, with the remainder in inorganic forms. Organic forms consist of dead plant/animal residues and soil microorganisms, which are crucial for converting them into plant-usable forms (Tapia-Torres and Garc´ıa-Oliva, 2013). However, soil microorganisms may hinder phos- phorus absorption through mineralization processes (Kwesi- Asomaning, 2020; Singh et al., 2015).
Phosphate rocks, essential for phosphorus compounds and fertilizers, are globally transported at a rate of approxi- mately 30 million tons annually. Morocco, with 85% of its reserves, extracts phosphorus from alkaline intrusive igneous rocks like apatite (Contrato, 2018; Azam et al., 2019). Despite finite resources, with about 100 years of reserves left, concerns arise about potential hoarding by major producers and its impact on global food security (Es- camilla, 2015). Apatite extraction may introduce high levels of heavy metals and radioactive elements, posing risks to biomass and disrupting carbon and nitrogen cycles (Bas´ılio et al., 2022).
Recycling organic materials, such as sewage sludge, Or- ganic Waste, invasive weeds, and agro-industrial residues, offers an alternative phosphorus source (Grigatti et al., 2017; Oliveira et al., 2019; Kauser and Khwairakpam, 2022; Herna´ndez-Lara et al., 2021; Zuhair et al., 2022). Stud- ies show that composted organic materials provide superior soil-available phosphorus compared to chemical fertiliz- ers (Adnan et al., 2017). Targeted recycling of Organic Waste and sludge is crucial for reintroducing nutrients into the soil, enhancing biofertilizer production, increasing agri- cultural output, and addressing public health, environmen- tal protection, and climate change concerns (Galvis, 2016; Herna´ndez-Berriel et al., 2016; Vergara and Tchobanoglous, 2012).
This review stems from the research question: What molecules present in organic matter wastes have the poten- tial to solubilize phosphates and how can they be managed through composting and its relationship to agricultural pro- duction sustainability? For this reason, the primary objec- tive of this work is to identify molecules present in organic matter that possess properties for phosphate solubilization and to explore the composting process of Organic Waste aiming to leverage the phosphorus (P) release capacity as an essential element for plant growth.
In a world where phosphorus availability is crucial for agri- cultural production, understanding how these molecules can influence phosphate solubilization could be key to improv- ing the efficiency and sustainability of fertilization systems. In this way, it could not only contribute to optimizing the use of natural resources but also to reducing the reliance on synthetic fertilizers and their potential environmental
‌impacts.

Materials and method

One hundred and eighteen articles were obtained from our search, which was conducted following the methodology proposed by Ferenhof and Fernandes (2016). We used Scopus, Science Direct, Web of Science, PubMed, Scielo, Google Scholar, ResearchGate, and Dialnet databases and considered articles published from 1972 to 2023. The search focused on the following keywords or topics: Phosphorus in the Earth’s crust, phosphorus recovery from Organic Waste, compost, metabolic pathways for phosphorus release in compost, and microbial activity for phosphorus release in compost.

In addition to composting, vermicomposting a process car- ried out by earthworms, principally the red Californian earthworm, (Eisenia fetida or Eisenia andrei) can also trans- form organic residues into compost. This process is more efficient for biologically treating pre-processed materials like livestock manure (Ferraz et al., 2022) since it promotes the metabolism of easily assimilable molecules, such as sim- ple carbohydrates, peptides, and proteins. It also increases P, Ca, and Mg levels through the mineralization process of the raw materials used.

Composts have regulations to ensure their quality and safety. In the European Union, Regulation (EU) 2019/1009 on solid organic fertilizers establishes the minimum parameter for P at 1 − 2% per mass of P2O5 (EU, 2019). In the specific case of Colombia, solid and liquid organic fertilizers must be endorsed by NTC 5167 (ICONTEC, 2011), which also requires reporting if the phosphorus concentration exceeds 1%, as this affects application to soil or crops.

The role of compost microbiota in P availability

The availability of phosphorus in both soil and organic residues is guided by phosphorus-solubilizing microorgan- isms (bacteria (BSP) and fungi (FSP) and Arbuscular Myc- orrhizal Fungi (AMF)), which are specifically responsible for solubilizing or mineralizing it (Fig. 1, Table 2). The principal BSPs for this function is Pseudomonas, Bacil- lus, Burkholderia, Kleibsella, Agrobacterium, Aeromonas, Rhizobium, Alcaligenes, Achromobacter, and Lactobacillus (Table 2), while the most representative groups of FSP are Aspergillus, Penicillium, Trichoderma, and Paecilomyces (Table 2). Most of these microorganisms belong to the rhi- zosphere of plants, but they can also be found in organic matter, which is the main component of organic residues. P solubilization and mineralization are performed by microor- ganisms through their metabolism, involving the extracellu- lar production of short-chain Organic Acids for inorganic phosphorus or enzymes for organic phosphorus (Fig. 1). Some microorganisms also perform other functions, such as promoting plant growth (Silva et al., 2023). Thus, their presence is valuable for agriculture.

Microorganisms not producing halozone for phosphorus solubilization may employ alternative mechanisms, such as siderophores, which chelate iron atoms from phosphate compounds. These siderophores are present in gram- negative bacteria, fungi, yeasts, and some plants (Aguado et al., 2012). In contrast, Gram-positive bacteria, known for their resilience to adverse conditions, may be more efficient in phosphate solubilization, particularly in withstanding pH changes during composting and in the soil (Corrales et al., 2014).

Arbuscular mycorrhizal fungi (AMF), including Acaulospora scrobiculata, Glomus deserticola, Glomus in- traradices, Glomus versiforme, Acaulospora morrowiae, Acaulospora spinosa, Gigaspora rosea, and Rhizophagus

intraradices (Table 2), establish associations in conditions of phosphorus (P) scarcity or immobilization due to the bind

with cations like Al, Fe, or Ca. These associations, found in approximately 80% of plant species, involve AMF extend-

‌Table 1. Chemical characterization of organic waste and sewage sludge.

		EC	OM	TOC		N	P	K
Origin Residues	pH	(dS/m)	%	%	C/N	%	%	%	References
OFMSW	7.27	2.06	85.43	40.29	15.20	2.65
WSW India AW	6.54 7.21	0.85 0.86	94.15 95.24	45.18 44.36	86.88 58.36	0.52 0.76	ND	ND	(Awasthi et al., 2015)
YW	7.39	0.74	93.14	40.72	45.75	0.89
CHD MOH MSW	ND	ND	58.92 58.27	34.18 33.80	25.30 22.10	1.35 1.53	ND	ND	(Rana et al., 2018)
PKL (India)			54.99	31.90	27.10	1.10
R1 Mauritius R2	7.40 7.30	0.29 0.26	81.37 65.68	47.20 38.10	27.00 25.40	1.70 1.50	ND	ND	(Soobhany, 2018)
(Africa) R3	7.20	0.19	73.09	42.40	27.20	1.60
CB			43.90	25.46	48.96	0.52	0.15	2.32
PJ Pombal (Brazil) PM	ND	ND	50.17 43.96	29.10 25.49	32.69 20.72	0.89 1.23	0.17 0.18	0.20 0.30	(Pedrosa et al., 2013)
SM			39.82	23.09	21.57	1.07	0.52	1.50
Paipa MOSW (Colombia)	ND	0.002	61.54	35.70	21.40	1.67	ND	ND	(Garc´ıa-Molano et al., 2021)
Ventaquemada (Colombia) RC	8.18	ND	77.58	45.00	19.90	2.26	ND	ND	(Boho´rquez-Sandoval et al., 2020)
United Kingdom MSW	6.10	4.90	38.70	ND	1.37	1.64	0.45	0.95	(Pascual et al., 1999)
AL	10.20	2.00	117.40	68.10	31.80	2.14	1.53
Italy SS	7.90	1.00	47.70	27.70	6.90	3.90	1.78	ND	(Grigatti et al., 2017)
GW	6.80	0.93	43.40	25.20	22.50	1.12	0.26
KW1	4.99		98.99	57.42	17.08	3.36	0.86
China S	7.02	ND	74.63	43.29	47.25	0.91	0.09	ND	(Wei et al., 2017)
MM	5.40		93.35	54.15	24.59	2.37	0.78
RS			85.85	49.80	94.20	0.53	0.05	1.07
WS			90.68	52.60	90.40	0.58	0.06	1.19
MS India CS	ND	ND	87.40 84.13	50.70 48.80	89.30 64.70	0.57 0.75	0.08 0.06	1.33 1.19	(Moharana et al., 2020)
TL			95.85	55.60	121.60	0.46	0.05	1.50
CD			64.30	37.30	60.20	0.62	0.14	1.11
Pakistan SPW	ND	ND	69.80	40.50	28.30	1.46	0.13	ND	(Billah and Bano, 2014)
KW2 China S	4.83 5.61	1.66 0.09	72.85 81.01	42.26 46.99	13.41 223.70	3.15 0.21	0.46 0.21	ND	(Zhan et al., 2021)

EC: electrical conductivity; OM: Organic matter; TOC: total organic carbon; N: total nitrogen; P: total phosphorus; K: total potassium CHD: Chandigarh, MOH: Mohali, PKL: Pankhula, OFMSW: Organic fraction of municipal solid waste, WSW: Wood chip waste, AW: Agricultural waste, YW: Yard waste, MSW: Municipal solid waste, R1: Food waste, R2: Paper waste, R3: Garden waste, CB: Banana peelings, PJ: Jurema pruning, PM: Marmeleiro pruning, SM: Sheep manure, MOSW: Municipal organic solid waste, RC: Rumen content, AL: Agro-industrial sewage sludge, SS: Urban sewage sludge, GW: Green waste, KW: Kitchen waste, S: Sawdust, MM: Mixed materials, RS: Rice straw, WS: Wheat straw, MS: Mustard stubble, CS: Chickpea stubble, TL: Tree leaves, CD: Livestock manure, SPW: Simple poultry waste.

‌Figure 1. Mechanisms for obtaining available plant P PSB: Phosphorus solubilizing bacteria, PSF: Phosphorus solubilizing fungi, AMF: Arbuscular mycorrhizal fungi.

ing their hyphae into the plant’s rhizosphere and penetrating the root cortex, serving various purposes. This includes increased nutrient absorption by the plant, exploration of a larger soil area, enhanced plant biomass, and the provision of organic carbon to AMF. Additionally, AMF contributes to soil stability by producing glomalin and Phytohormones that facilitate P availability to the plant (Maaloum et al., 2020; Etesami et al., 2021; Garc´ıa-Molano et al., 2022; Perea et al., 2019; Velzquez et al., 2017; Wahid et al., 2020). This mycorrhizal association depends on phosphate-solubilizing fungi (PSF) and, to a lesser extent, phosphate-solubilizing bacteria (PSB) (Fig. 1), which play a crucial role in facil- itating interactions between AMF and plant roots. These interactions involve chemical pathways for P solubilization, accomplished through PSF production of low molecular weight Organic Acids or enzymes and hormone secretion. Furthermore, AMF exude fructose, activating phosphatase genes in PSB and promoting organic phosphorus mineraliza- tion (Maaloum et al., 2020; Etesami et al., 2021; Ordon˜ez et al., 2016). Compost, with organic molecules resembling plant exudates, supports AMF nutrition and growth, fa- cilitating effective P transport to plants. For this reason, when applied to the soil, compost can likely promote mycor- rhizal associations, considering its nutritional contributions to AMF (Yang et al., 2018).

Enzymatic activity (phosphorus mineralization)

Mineralizing organic phosphorus to release orthophosphates occurs when various microbial groups produce extracellular enzymes that synthesize three hydrolytic enzymes: i. phos- phonoacetaldehyde hydrolase (phosphonatase), ii. phospho- noacetate hydrolase, iii. phosphonopyruvate hydrolase; iv. C-P lyase breaks the C-P bond, releasing phosphate ion (HPO4-2) from the organic P source (Kaur, 2020; Tapia- Torres and Garc´ıa-Oliva, 2013). Pyrophosphatase also hy- drolyzes pyrophosphates, which are a group of polyphos- phates (Darch et al., 2016). Similarly, non-specific phos- phatases dephosphorylate P in phosphorylated proteins, and phytases release P from phytic acid (Kaur, 2020). The latter is mainly produced by species of the Bacillus and Enterobacter genus, which have the advantage of operat- ing within pH ranges of between 3.5 and 7.5 but are more efficient under alkaline pH. Likewise, within the group of

phytases, the β -helix phytase should be highlighted for its exceptional phosphate solubilizing activity (Corrales et al., 2014), along with species from the genera Pseudomonas sp., Burkholderia sp., Alcaligenes sp., and Aspergillus sp., which mineralize P by producing phosphatases and phytases (Babana et al., 2013; Behera et al., 2017; Bol´ıvar-Anillo et al., 2016; Cheng and Wan, 2022).

Organic acids (phosphate solubilization)

Fungi and bacteria play a crucial role in phosphate solubi- lization, a process influenced by pH, organic matter inter- actions, and soil physicochemical characteristics (Babana et al., 2013; Darch et al., 2016). The type of organic acid produced depends on pH, with compost pH being alkaline. Adjusting compost pH to 5.0 enhances organic acid and enzyme efficiency (Darch et al., 2016), however, Marra et al. (2015) propose that organic acid production is pH- independent, and it is mediated by mechanisms like proton exclusion, siderophores, and exopolysaccharide production. Phosphate-solubilizing microorganisms (PSM), produce or- ganic acids from macromolecules like carbohydrates, lipids, and peptides through a fermentative pathway like glycoly- sis (Beltra´n-Pineda, 2015; Paredes-Mendoza and Espinosa- Victoria, 2009). Gluconic acid is produced by Penicillium rugulosum from glucose or sucrose, and Aspergillus niger produces citric acid through sucrose fermentation (Pe´rez- Navarro et al., 2016). Gluconic acid releases phosphorus from Ca-P bonding, while oxalic acid releases P from Fe- P and Al-P, acting as chelating agents for these cations (Beltra´n-Pineda, 2015). Microorganisms like Pseudomonas sp. and Penicillium sp. produce citric acid, the most ef- ficient organic acid in phosphate solubilization (Babana et al., 2013). Bacteria of the Bacillus genus use different pathways, including tricarboxylic acids, to synthesize malic acid or direct glucose oxidation to produce 2-ketogluconic acid (Table 2) (Corrales et al., 2014). Also, certain bacte- ria, which produce the enzymatic cofactor pyrroloquinoline quinone (PQQ), are known to contribute to the synthesis of organic acids such as gluconic acid, (Sarr et al., 2020; Vera-Cardoso et al., 2017). Fungi present in compost, de- spite their smaller population, exhibit higher efficiency in P solubilization, attributed to their production of a larger quan- tity of organic acids compared to bacteria (Babana et al., 2013). On the other hand, the direct action of phosphorus genes on the solubilization of minerals containing it is well established, involving genes such as gcd, ppx, and ppa for Pi, and genes like phoA, phNW, phoD, phnP, phnl, phnG, and phnJ for Po (Xu et al., 2023).

Phytohormones

Phosphate solubilization can also be attributed to phytohor- mone secretion by various microorganisms from the gen- era Pseudomonas, Bacillus, Azotobacter and Azospirillum. These groups are of interest for phosphate solubilization and also have characteristics such as fixing nitrogen, producing phytohormone, and promoting plant growth (Licea-Herrera et al., 2020). The main Phytohormones studied for phos- phorus (P) solubilization include auxins, which promote lateral root production for nutrient absorption while inhibit- ing primary root growth; ethylene, involved in forming ad-

ventitious roots under P deficiency and linked to acid phos- phatase regulation (Bas´ılio et al., 2022); and strigolactones, inducing morphological, physiological, and biochemical changes in plants. Strigolactones contribute to increased root biomass, aiding in soil P scavenging through symbiosis with fungi in mycorrhizal formations. Strigolactones may also acidify the environment by releasing protons from root exudates, working in conjunction with phytase and acid phosphatase. However, excess P in plants can negatively impact strigolactone synthesis, reducing dissolved organic carbon exudation (Santoro et al., 2021). Although research on the role of Phytohormones in P solubilization in compost is in its early stages, it highlights another mechanism ben- efiting organic residues and sludge, not only as a nutrient source for the soil but also as a source of microorganisms, fostering synergistic relationships between microorganisms

and plants.

Phosphorus fractions in composts from organic waste and sludge

Phosphorus forms in organic wastes and sludge com- posts

Phosphorus in compost can be present in different forms:

i. labile, corresponding to orthophosphates that are easily assimilated by plants; ii. moderately available phosphorus, which is bound to metals such as Fe, Al, and Ca and can be solubilized through organic and inorganic acids, along with organic phosphorus as phosphate esters that can be mineralized by enzymes to convert it into labile phosphorus; and iii. occluded phosphorus, which is present in molecules that are challenging to solubilize and mineralize (Takahashi and Dahlgren, 2016; Tinoco-Varela and Bayuelo-Jime´nez,

‌Table 2. Phosphorus-solubilizing microorganisms involved in phosphate solubilization, mineralization, and transport

Type Microorganism P solubilization mechanisms References

Bacteria

Aeromona salmonicida

Pasteurella pneumotro´pica Alcaligenes sp.

Indoleacetic acid (IAA) Alkaline phosphatase enzyme

Organic acids and phosphatase

(Pe´rez-Cordero et al., 2014) (Behera et al., 2017)

Bacteria Burkholderia tropica

Gluconacetobacter diazotrophicus Herbaspirilum seropedicae

enzymes.

Plant growth promoter (PGP) and siderophore.

(Bol´ıvar-Anillo et al., 2016) (Corrales et al., 2014)

(Restrepo-Franco et al., 2015)

Bacteria

Paenibacillus lautus Herbaspirillum sp. Azospirillum sp.

Azotobacter sp Pseudomonas sp.

P. aeruginosa Rhizobium, Burkholderia sp, Achromobacter sp Agrobacterium, Aereobacter Flavobacterium Yarowia, Streptosporangium Erwinia herbicola Proteus

Pantoea Mycobacterium Anthrobacter Enterobacter Bacillus sp.; B liqueniformis

B. amyloliquefaciens; B. megaterium; B. firmus Brevibacillus sp Lactobacillus sp Herbiconiux sp Halopolyspora sp Cosenzaea sp Aeromicrobium sp Cellulosimicrobium sp Lentibacillus sp Klebsella sp.; K. oxytoca Micrococcus sp Agrobacterium tumefaciens

Phytohormones IAA. PGP

PGP

Organic acids, phosphatase enzymes, and, in some cases, phytases.

Organic acids, phosphatase, and phytase enzymes.

PGP.

Organic acids.

Mobilization of organic and inorganic P.

Organic acids.

(Bas´ılio et al., 2022)

(Pe´rez-Pazos and Sa´nchez-Lo´pez, 2017)

(Babana et al., 2013)

(Paredes-Mendoza and Espinosa-Victoria, 2009) (Billah and Bano, 2014)

(Zhang et al., 2021)

(Estrada-Bonilla et al., 2017) (Zhang et al., 2018)

(Adnan et al., 2017)

(Estrada-Bonilla et al., 2017) (Yadav et al., 2017)

(Zhang et al., 2021) (Zhan et al., 2021) (Adnan et al., 2017)

(Estrada-Bonilla et al., 2017) (Zhan et al., 2021)

(Zhan et al., 2021) (Babana et al., 2013)

Bacteria

Firmicutes

Proteobacteria Bacteroidetes Bacillus sp.

Organic acids. (Wei et al., 2017)

(Castillo-Arteaga et al., 2016)

Bacteria

B. megaterium

B. subtilis

B. cereus Pseudomonas sp, Pantoea, Mycobacterium

Organic acid.

(Panhwar et al., 2013) (Saeid et al., 2018)

Bacteria

Haloarchaea

Bacillus, Rhizobia, Burkholderia,

Arthrobacter Enterobacter Rhizobium tropici Acinetobacter sp.

Paenibacillus kribbensis Haloarcula argentinensis; Halobacterium sp.; Halococcus sp.; Halococcus hamelinensis; Haloferax sp., H. alexandrines; H. larsenii;

H. volcanii Halolamina sp.; Halolamina pelagic; Halosarcina sp.;

Halostagnicola kamekura;, Haloterrigena sp.

Aspergillus niger; Penicillium pinophilum;

Organic acids. (Adnan et al., 2017)

Organic acids. (Marra et al., 2015)

Organic acids. (Yadav et al., 2015)

(Chuang et al., 2006)

Fungi

Talaromyces rotundus; Penicillium pimiteouiense; Acremonium strictum;

Penicillium chrysogenum; Aspergillus awamori

Aspergillus niger; Aspergillus flavus; Trichoderma harzianum

Organic acids.

Organic acids. Phosphatase and phytase enzymes.

Enzymes: phytase, acid phosphatase + phytase; carboxymethyl cellulase + phosphatase.

(Klaic et al., 2017)

(Babana et al., 2013)

(Gaind, 2014)

Fungi Paecilomyces lilacinus Organic acids. (Herna´ndez-Leal et al., 2011)

Fungi

Aspergillus niger; Penicillium brevicompactum Acaulospora scrobiculata;, Glomus sp.;

Enzymes: phytases. (Perea et al., 2019) Organic acids.

Enhances the uptake of

AMF

G. desert´ıcola;

G. intraradices;

G. versiforme

soluble phosphates in mycorrhizal association.

Enhances the uptake of

(Maaloum et al., 2020)

AMF Rhizophagus intraradices

Acaulospora morrowiae; Acualospora spinose; Acualospora scrobiculata; Gigaspora rosea;

soluble phosphates in mycorrhizal association.

Enhances the uptake of

(Velzquez et al., 2017)

AMF

Scutellospora pellucida; Glomus macrocarpum; Funneliformis mosseae; Funnelliformes geosporum; Rhizophagus aggregatus;

soluble phosphates in mycorrhizal association.

(Perea et al., 2019)

‌Table 3. Total P and bioavailable P values in different types of compost and vermicompost

Total phosphorus Bioavailable			Reference
		(g/kg)
Urban solid organic waste	1.99	ND	(Garc´ıa-Molano et al., 2021)
Wastewater sludge	6.00	2.51	(Grigatti et al., 2017)
Rice straw	8.50	0.90
Wheat straw	7.80	0.80
Mustard stubble	6.10	0.75	(Moharana et al., 2020)
Chickpea stubble	6.50	0.70
Tree branches	6.30	0.62
Poultry litter without inoculation	230.00	9.69
Poultry litter with Pseudomonas sp.	410.00	17.20	(Billah and Bano, 2014)
Poultry litter with Proteus sp.	300.00	12.40
Pig manure	21.95	6.08
Chicken manure	29.99	8.64
Municipal solid waste	6.76	1.17	(Wei et al., 2015)
Kitchen waste	3.36	0.78
Green waste	4.62	1.86
Rice straw with pig manure	1.34	ND	(Chen and Wan, 2023)
Municipal solid waste	3.00	ND	(Ahmadi et al., 2020)
Organic waste	2.10	ND	(Sandoval et al., 2020)
Organic fraction of urban solid waste	5.40	ND	(Saldarriaga et al., 2018)
Agro-industrial waste	3.20-8.90	ND	(Herna´ndez-Lara et al., 2021)
Kitchen waste	4.58	0.59	(Zhan et al., 2021)
Ruminal content	15.10	ND	(Boho´rquez-Sandoval et al., 2020)
Grape pomace waste:	0.75

Composts

(TP) (g/kg)

phosphorus (PAV)

Almarin˜o variety 1.41 ND			(Go´mez-Brando´n et al., 2021)
Mixture of weed waste, manure, and sawdust	12.87	ND	(Kauser and Khwairakpam, 2022)
Agro-industrial poultry waste	16.90	ND	(Niedzialkoski et al., 2021)
Vineyard waste	2.00	ND	(Blaya et al., 2013)
Inoculated residual municipal solid waste with PSB	10-18	4.20-8.10	(Wei et al., 2017)
Rice straw and PR	24.20	1.15
Wheat straw and PR	22.70	1.08
Mustard stubble and PR	21.00	1.08	(Moharana et al., 2020)
Chickpea stubble and PR	21.60	1.08
Tree branches and PR	20.90	0.95
Kitchen waste with PR 5%	20.63	0.29
PR 10%	31.16	0.74	(Zhan et al., 2021)
PR 15%	40.64	0.45
Mixture of manures: Cattle, horse, and poultry,
adding PR in three concentrations:	145.00	1.60
Compost with 5% PR	151.00	1.65	(Pa´ez et al., 2022)
Compost with 10% PR	215.00	1.70
Compost with 15% PR
Vineyard waste: 1.50		ND	(Blaya et al., 2013)
Plant and animal waste with Azospirillum brasilense inoculation	ND	12.00 (Hafez et al., 2021)
Rice straw + cattle manure	ND	0.62
Rice straw + farmyard manure	ND	0.74
Rice straw + poultry manure	ND	1.48 (Gaind, 2014)
Rice straw + cattle manure + PSF	7.12	0.85
Rice straw + farmyard manure + PSF	6.70	0.85
Rice straw + poultry manure + PSF	9.98	1.56

Menc´ıa variety

With Trichoderma harzianum inoculation

PR: Phosphate rock; PSF: Phosphate-solubilizing fungi; PSB: Phosphate-solubilizing bacteria.

2021; Velzquez et al., 2017). The phosphorus absorbed by plants is mineralized organic phosphorus, which originates from phosphate esters where P is bound to oxygen in its maximum oxidation state (+5), making it highly suscepti-

ble to mineralization. There are also phosphonates, where phosphorus is directly bound to carbon, forming bonds that require more energy to break, operating with an oxidation state of +3 (Tapia-Torres and Garc´ıa-Oliva, 2013).

Quantification methods of Phosphorous forms

Various methodologies for extracting plant-available P have been developed, among which the most relevant are Colwell (1963), Bray I and II (1945), Mehlich (1984), and Olsen- P (1954); the latter being the most widely used analytical method (Milham et al., 2023). Moharana et al. (2020) indi- cate that this method is commonly used due to its response to different substrates, making it a good indicator of plant- available P; In some cases, another indicator of availability is citric acid-soluble P at 2% for acidic media (CASP); it is also important to determine the percentage of P solubi- lization. In response to this, the European Commission proposed the SMT (Standards, Measurements, and Testing) method, which analyzes total phosphorus (TP), inorganic phosphorus (Pi), organic phosphorus (Po), non-apatite phos- phorus (NAP), and apatite phosphorus (AP), aiming for uniformity in fractionation methods (Ruban et al., 2001; Garc´ıa, 2014; Velasco, 2021).

Phosphorus availability in organic waste composts

The content and availability of phosphorus in composts can increase during the composting process, as indicated by Cheng and Wan (2022), 2023. For instance, compost made from sorghum straw and pig manure exhibited an increase from an initial phosphorus content of 0.5 g/kg to 1.34 g/kg after composting (Table 3). The phosphorus content in com- posts is influenced by the raw materials used, suggesting that combining various materials can enhance the macronu- trient values (Table 3). This results in increased phosphorus content and promotes microorganisms involved in solubi- lization or mineralization, facilitating the gradual release of phosphorus and preventing losses through leaching or chelation (Vicentin et al., 2021).

Ortega (2022) demonstrated the production of enzymes like phytases, acid phosphatases, alkaline phosphatases, and neutral phosphatases by inoculating Pseudomonas aerug- inosa into cattle manure compost. This led to the re- lease of orthophosphate ions, highlighting the synthesis of various enzymes with mineralizing functions. Wan et al. (2021) showed that alkaline phosphatase activity was intense toward the end of composting, potentially favoring increased available phosphorus from organic waste. How- ever, other Enzymatic activities, such as β -1,4-glucosidase, β -D-fructofuranosidase, β -1,4-N-acetylglucosaminidase, and sulfatase, may also influence phosphorus availability, although this relationship has not been extensively studied. Wei et al. (2018b) and Wei et al. (2018a) found that formic acid exhibited the most solubilization activity for various forms of phosphorus, including TP, Po, Pi, Olsen-P, PAC (phosphorus soluble in citric acid), and microbial biomass phosphorus (MBP). Oxalic acid acted on TP, Po, Pi, and MBP, while citric acid influenced Po and MBP. These ac- tivities occurred during the cooling phase of composting, suggesting that the Organic acids, available phosphorus, and phosphate-solubilizing microorganisms reached the soil, en- hancing plant activity.

The total phosphorus content in composts varies depend- ing on the source material, ranging from 2 to 9 g/kg for composts derived from organic waste, sludge, and agro-

industrial wastes, to 14 to 17 g/kg for composts produced from manures or animal wastes (Table 3). Post-composting, phosphorus tends to accumulate, with substrate influencing microbial community establishment, particularly in animal manure composts, where phosphorus levels can reach 34 kg/ton (Williams, 2013). However, the majority of avail- able phosphorus comes from organic matter, with content varying based on phosphorus form, carbon, and nitrogen levels (Herna´ndez-Leal et al., 2011). Understanding the native microbiota of composted materials is essential for en- hancing process efficiency (Gaind, 2014). Wei et al. (2016) identified key phylogenetic groups involved in phosphorus transformation, such as Firmicutes, Proteobacteria, and Bacteroidetes, which contribute to the formation of slow- release phosphorus sources for plants. Families like Pseu- domonadaceae, Enterobacteriaceae, and Bacillaceae are capable of solubilizing phosphorus in soils and are com- monly found in composts and plant rhizospheres. Greater raw material diversity corresponds to increased microbial diversity and enzyme production. When compost is applied to the soil, it promotes mineralization processes of organic phosphorus in the soil’s organic matter, laying the founda- tion for developing techniques to isolate microorganisms synthesizing phosphatases for use as biofertilizers.

The total phosphorus content or availability in composts inoculated with phosphate-solubilizing microorganisms (PSMs) varies based on the raw material type and spe- cific PSMs used. Billah and Bano (2014) observed su- perior outcomes with the phosphate-solubilizing bacterium Pseudomonas sp., compared to Proteus sp. and the con- trol without inoculation, resulting in increased plant height and grain production. Biochar + oil palm bunch compost applied to maize crops fosters populations of phosphate- solubilizing fungi like Aspergillus sp. and Neosartorya sp., enhancing microorganism adaptability and promoting maize growth through increased phosphorus absorption. This medium increased phosphorus absorption in maize plants by 100 −200%, promoting their growth by producing various compounds. Chen and Wan (2023) highlighted the challenges of decomposing residues with high lecithin levels and demonstrated the mineralization of organic phosphorus (Po) by the WWJ-22 strain of Pseudomonas sp., leading to increased phosphorus availability. Yadav et al. (2017) demonstrated that compost from various sources, including agricultural wastes and manure, with added phosphate rock (PR) and inoculated heat-resistant phosphate-solubilizing bacteria (Brevibacillus and Bacillus) in wheat cultivation, resulted in elevated total phosphorus levels, shoot and root length, and plant biomass. They emphasized compost as a conditioning medium for phosphate-solubilizing bacteria (PSB), essential for slowly solubilizing phosphorus for plant growth. Babana et al. (2013) compared the solubilization of Tilemsi phosphate rock using bacteria (Pseudomonas sp. and Vibrio splendidus) and fungi (Penicillium chrysogenum thom and Agrobacterium tumefaciens) isolated from wheat rhizospheres. Bacteria showed a higher solubility index, but fungi had more elevated solubilized phosphorus (Sarr et al., 2020). The latter demonstrated that heat-resistant phosphate-solubilizing fungi, by the end of composting,

had a stronger correlation with labile phosphorus (labile-P) and total phosphorus (TP) than bacteria, along with a higher correlation with alkaline phosphatase activity.

Gaind (2014) observed the concentration of mineralized phosphorus (Po), as measured by Olsen-P, doubling the phosphorus compared to the control treatment in different types of composts (rice straw with poultry manure, rice straw with cattle manure, and rice straw with farmyard ma- nure) inoculated with a consortium of fungi (Aspergillus niger, Aspergillus flavus, and Trichoderma harzianum). In another study, Hafez et al. (2021) inoculated the bacterium Azospirillum brasilense into organic ecological waste com- post, resulting in a notable increase in labile phosphorus, highlighting the role of indoleacetic acid (IAA) metabolic pathways in facilitating phosphorus solubilization and en- hancing crop production (Table 3).

Additionally, vermicomposting of organic waste contributes phosphorus (P) as an organic fertilizer, facilitated by the mineralization of organic phosphorus within the earth- worm’s digestive tract and the production of enzymes like phosphatases and phytases. Studies by Boho´rquez-Sandoval et al. (2020) and Go´mez-Brando´n et al. (2021) demonstrated increased total phosphorus (TP) content in vermicomposts derived from different organic materials. Combining com- posting with vermicomposting has also been explored, re- vealing promising phosphorus levels in the mix (Kauser and Khwairakpam, 2022; Niedzialkoski et al., 2021; Zuhair et al., 2022).

Yang et al. (2018) found that cattle manure and maize stalk compost applied to soybean cultivation increased the density of arbuscular mycorrhizal fungi (AMF) spores and hyphae. This enhancement favored the flowering and maturation phases of the crop, regardless of the quantity of compost added. These findings suggest that the fungal spores belong to the native soil population of the Glomeraceae family. They highlighted that root colonization is influenced by the soybean crop’s demand for substantial amounts of phospho- rus (P) for atmospheric nitrogen fixation. Furthermore, the hyphae promote a slow and sustained release of labile P for the plant.

microorganisms (PSM), their contents can increase as these microorganisms are involved in their solubilization. There are different mechanisms of P solubilization, such as Organic acids, phosphatases, symbiotic relationships, microbial interactions, and the action of phosphorus-related genes, which increase its slow release, reducing the use of highly soluble sources.

Author contribution

The authors confirm the conception and design of the study: Boho´rquez-Sandoval LJ, Garc´ıa- Molano JF, Pascual-Valero JA, and Ros-Mun˜oz M; data collection: Boho´rquez-Sandoval LJ, Garc´ıa-Molano JF; analysis and interpretation of results: Boho´rquez-Sandoval LJ, Garc´ıa-Molano JF, and Ros-Mun˜oz M; preparation of the pre- liminary manuscript: Boho´rquez-Sandoval LJ, Garc´ıa-Molano JF. The results were evaluated by all authors, and the final version of the manuscript was approved. The authors and contribution to the research effort adhere to the authorship standards established in the IJROWA Authorship Guidelines and as advised by the Committee on Publication Ethics (COPE).

Availability of data and materials

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Conflict of interest statement

The authors declare that they are no conflict of interest associated with this study.

Open access

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the OICC Press publisher. To view a copy of this license, visit https://creativecommons.org/licenses/by/4.0.\

Conclusion

The need to find alternative sources of P to maintain sustainable agriculture has turned organic waste composts and sewage sludge into a nutrient source to reduce the use of inorganic sources. Depending on the raw materials used, and also due to the incorporation of phosphorus-solubilizing

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A comprehensive review on organic waste compost as an effective phosphorus source for sustainable agriculture

Review Paper

Abstract:

Keywords: Enzymatic activity; Organic acids; Organic waste; Phytohormones; Phosphate solubilizers

‌Introduction

Materials and method

The need for new sources of Phosphorus in agriculture

Phosphorus recovery from organic waste and sewage sludge

Phosphorus recycling from OW and sewage sludge: Composting

The role of compost microbiota in P availability

‌Table 1. Chemical characterization of organic waste and sewage sludge.

Enzymatic activity (phosphorus mineralization)

Organic acids (phosphate solubilization)

Phytohormones

Phosphorus fractions in composts from organic waste and sludge

Phosphorus forms in organic wastes and sludge com- posts

‌Table 2. Phosphorus-solubilizing microorganisms involved in phosphate solubilization, mineralization, and transport

‌Table 3. Total P and bioavailable P values in different types of compost and vermicompost

Quantification methods of Phosphorous forms

Phosphorus availability in organic waste composts

Author contribution

Availability of data and materials

Conflict of interest statement

Open access

Conclusion

References