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Article

Sustainable Use of Organic Seaweed Fertilizer Improves the Metagenomic Function of Microbial Communities in the Soil of Rice Plants

by
Eka Sunarwidhi Prasedya
1,2,*,
Nanda Sofian Hadi Kurniawan
1,
Fitriani Fitriani
2,
Putu Bella Aprillia Saraswati
2,
Wanda Qoriasmadillah
2,
Bq Tri Khairina Ilhami
1,
Ari Hernawan
1,3 and
Sri Widyastuti
1,4
1
Bioscience and Biotechnology Research Center, University of Mataram, Mataram 83126, Indonesia
2
Department of Biology, Faculty of Mathematics and Natural Science, University of Mataram, Mataram 83126, Indonesia
3
Department of Informative Technology, Faculty of Engineering, University of Mataram, Mataram 83126, Indonesia
4
Faculty of Food Technology and Agroindustry, University of Mataram, Mataram 83126, Indonesia
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(23), 16328; https://doi.org/10.3390/su152316328
Submission received: 9 October 2023 / Revised: 18 November 2023 / Accepted: 21 November 2023 / Published: 27 November 2023
(This article belongs to the Section Sustainable Agriculture)
Browse Figures
Versions Notes

Abstract

:
The frequent use of chemical fertilizers in agricultural practices has developed into a serious environmental concern which urgently needs a solution to restrain their use in agricultural systems. Hence, there is an urgent need to investigate potential organic fertilizers from various natural resources to decrease the use of chemical fertilizers. Seaweed is among the natural resources with potential sustainability value. Our previous work has shown the effectiveness of seaweed fertilizer for increasing plant growth and soil beneficial microbiota. This study aims to evaluate the functional genes present in the soil of rice plants treated with seaweed fertilization. It involves amendments with reduced concentrations of chemical fertilizer in three groups: CF (only chemical fertilizer), CFSF1 (50% dose of CF + seaweed fertilizer 1 ton/ha), and CFSF2 (50% dose of CF + seaweed fertilizer 2 ton/ha). The rice plants supplemented with CFSF1 and CFSF2 were taller and faster to mature compared to CF. In addition, the primary macronutrients nitrogen (N), phosphorus (P), and potassium (K) were also significantly higher in soil supplemented with SF. Our findings showed increased ammonia-oxidizing archaea Crenarchaeota abundance in increasing SF treatments. The PICRUSt analyses indicated enriched functional genes and proteins in relation to amino acid, nucleotide, protein, and carbohydrate metabolism based on the KEGG, BioCyc, and PFAM databases. The current outcomes enhanced our understanding regarding the importance of microbial community for soil quality. Furthermore, seaweed supplementation has shown improvement in soil fertility, which significantly increases rice plant growth and productivity.

Graphical Abstract

1. Introduction

Rice (Oryza sativa L.) is the most popular staple food of half of the world’s population and more than 90% of Indonesia’s population. However, in recent years, the trend between rice supply and demand in Indonesia has been the opposite. It could be predicted that rice demand would likely increase due to the increase in human population. On the contrary, the production of the nation’s rice is steadily decreasing [1]. In fact, Indonesia has had to import more than three million tons of rice annually to meet the market demands.
There are several factors which caused the steady decline of Indonesia’s rice production, such as unpredictable weather due to climate change and soil fertility [2]. The decline of soil fertility further causes the excessive use of fertilizers to support the sufficient growth of crops. This is an inevitable cycle which was caused by the long-term excessive usage of chemical fertilizers [3]. Hence, there is a growing urgency to find alternative solutions to reduce the amount of chemical fertilizers applied in agricultural practices. One promising solution is the development of organic fertilizers as a substitute for chemical fertilizer. The use of organic fertilizers has been reported to improve soil fertility, allegedly by restoring the beneficial bacterial community needed in the soil to sustain plant growth [4].
Among various organic fertilizers, seaweed-based organic fertilizers are considered to be environmentally friendly and also cost-effective [5]. The application of seaweed-based fertilizers has demonstrated improved productivity in various crops, including tomato, sugarcane, maize, wheat, and paddy [6,7,8,9,10]. Generally, seaweed contains essential minerals such as irone, iodine, manganese, calcium, nitrogen, phosphorus, sulphur, boron, potassium, and other elements which are essential to support plant growth [11]. Our previous work has also shown that supplementation of brown seaweed Sargassum-based fertilizer could increase growth and rice productivity and nutritional quality [12,13]. Until now, the brown seaweed Sargassum has not yet been cultivated in Indonesia. On the contrary, it often is referred to as a pest for commercial seaweeds such as the carrageenan-producing seaweeds Kappaphycus and Eucheuma. Hence, bioprospecting of these brown seaweeds as biofertilizers potentially bridges the gap in sustainable production between agricultural and aquaculture systems.
A common use of organic fertilizer is to increase soil fertility by increasing the mass and diversity of the soil microbiota [14]. Various studies have shown that the soil microbiota plays a vital role in improving soil health, quality, and fertility, whereas all of these factors are known to have a significant impact on agricultural product quality and yield [15]. Application of seaweed fertilizer has been shown to increase beneficial soil microbiota in plants [8,12,16]. Another study also showed that seaweed-fertilizer-structured microbial communities contribute to increased productivity in tomato and pepper plants [17].
Various studies have shown the effects of organic fertilizer application on shaping the soil microbial community [18,19]. However, there are limited studies showing the effects on the functional genes of these beneficial microbial communities. The use of bioinformatic methods such as PICRUSt (Phylogenetic Investigation of Communities by Reconstruction of Unobserved States) to offer more information about the functional genes involved in the microbial community is extremely promising [20,21]. This study intends to evaluate the potential of seaweed-based fertilizers in shaping the functional genes of the soil microbiota communities in agricultural systems.

2. Materials and Methods

The seaweed fertilizer (SF) was prepared according to methods described in a previous study [12]. The main composition of the fertilizer was of a mixture of brown seaweeds Sargassum spp. The biomass of the brown seaweed was fermented with commercial starter bacteria EM4 (1 L/ton) for 40 days [22]. The resulting fermented seaweed biomass was used as a solid fertilizer which was applied as a basal medium to the soil before transplantation of paddy experimental fields. The study was carried out in an experimental model paddy field site exposed to natural daily sunlight located at West Lombok (8°33′59.2″ S 116°09′56.2″ E) during the rainy season of December 2022 to March 2023. The physiochemical properties of the soil are shown in Table 1. The climate is classified as tropical, with an average annual rainfall of 144 mm and an average temperature of 34 °C.

2.1. Field Experimental Design

The fertilizer treatments were classified into 3 groups: chemical fertilizer treatment only (CF), 50% chemical fertilizer combined with 1 ton/ha seaweed fertilizer (CFSF1), and 50% chemical fertilizer combined with 2 ton/ha seaweed fertilizer (CFSF2) (Table 2). The CF treatment consisted of 300 kg/ha urea (CON2H4), 100 kg/ha trinatrium phosphate (Na3PO4), and 100 kg/ha potassium chloride (KCl), which was accordant with the regulations of the Indonesian Ministry of Agriculture. The CFSF1 and CFSF2 group both contained chemical fertilizer but the concentration was decreased to 50% (150 kg/ha CON2H4, 50 kg/ha Na3PO4, and 50 kg/ha KCl).
In addition, the application of CF in all treatment groups was performed twice, during the 10th (early rice) and 30th (late rice) days after paddy plant transplantation into the field treatment area. The field trial area was 0.02 ha (2 ares) wide for each treatment (Figure 1).

2.2. Determination of Rice Productivity

The crop was harvested based on the required time for the rice variant (Inpari 32) to mature in favorable conditions, which is approximately 110 days. Post harvest, the rice plant height, tiller number, and grain weight of each treatment were evaluated.

2.3. Determination of Soil Macronutrient Properties

The soil samples were collected from the top layer (±15 cm) and pooled from 10 random points from each field plots after harvest. The soil samples were left to dry at room temperature for 3–4 days. After drying, the soil samples were sieved (2 mm) to remove unwanted debris which could interfere with downstream analyses. The organic matter was quantified using the dichromate wet oxidation technique, as described by Walkley and Black. The total N was calculated using the micro-Kjehdal technique. The remaining macronutrients, P and K, were determined with ICP-OES.

2.4. Soil DNA Isolation and 16S rRNA Gene Amplification

The soil samples were taken during the harvest of the rice plants, which was around the 100th day after paddy transplantation in the field experimental area. Soil cores from 10 random points (approximately 15 cm from the top layer) from each field plot were collected with a teaspoon from each treatment and sampled and pooled in sterile 50 mL falcon tubes. The collected soil samples were stored in an ultralow freezer (−80 °C) for further analyses. The DNA soil samples were isolated according to a PureLink microbiome DNA purification kit (Invitrogen, lot. No. 1761498). The isolated DNA samples were subjected to a quality check (QC) which consisted of yield and purity (A260/280) using a NanoDrop1000 spectrophotometer (Thermoscientific, Wilmington, DE, USA). All samples should exceed the minimum concentration of 20 ng/µL and purity of 1.8–2.0 for NGS analyses. The hypervariable region V3–V4 of the 16S rRNA gene was identified to determine to the microbial communities of each treatment. The Phusion High-Fidelity PCR Master Mix (New England Biolabs, Ipswich, MA, USA) was used for all PCR experiments. For detection, we employed a volume of 1 loading buffer (including SYBR green) with PCR products and electrophoresis on a 2% agarose gel. For further analysis, samples with a bright main band between 400 and 450 bp were chosen. The PCR products that were chosen were combined at identical density ratios. The Qiagen Gel Extraction Kit (Qiagen, Hilden, Germany) was used to purify the mixed PCR products. The libraries were created using the NEB Next UltraTM DNA Library Prep Kit for Illumina and quantified using Qubit and Q-PCR for illuminated platform studies.

2.5. Taxonomic Identification and Prediction of Functional Genes

Based on unique barcodes, each sample was assigned with the paired-end reads. Together with the primer sequences, the barcode sequence was truncated. The reads were then merged to obtain raw tags using the FLASH software (v1.2.11, http://ccb.jhu.edu/software/FLASH/) (accessed on 1 August 2023). Quality checks (QCs) of the raw tags were conducted using fastp software (accessed on 1 August 2023). Finally, the effective tags were obtained via removal of chimeras with the Vsearch software 2.22.1. The software QIIME2 (Version 2021.4) was used to denoise the effective tags. The final ASVs (Amplicon Sequence Variables) were obtained by filtering out the sequence below the proscribed threshold. Using the Classify-sklearn module in QIIME2, the species annotations of each ASV were obtained. For functional prediction analyses, PICRUSt was used. The full name of PICRUSt is Phylogenetic Investigation of Communities (PICRUSt) based on the OTUs and gene information of OTUs in the KEGG, BioCyc, and PFAM databases. The composition of bacteria and archaea groups obtained via sequencing was ‘mapped’ to the database so as to predict the metabolic function of the microbiota group.

2.6. Statistical Analyses

To determine the significant differences between treatments, the analyses of variance (ANOVA) accompanied by multiple comparison. All statistical analyses were performed using the GraphPad Prism software version 10.1.0. The sequencing output was processed using QIIME2. In addition, Adonis analyses were also used to determine significant differences in the microbial community structure among treatment groups.

3. Results and Discussion

Seaweed fertilizer (SF) supplementation in rice fields were applied in two doses, which were 1 ton/ha and 2 ton/ha. The seaweed fertilizer was applied as a basal fertilizer before plantation. Based on our previous results, the application of SF combined with a reduced concentration of chemical fertilizer (CF) could significantly increase paddy plant growth [12]. The fertilizer treatments were applied in three groups: CF = chemical fertilizer only, CFSF1 = 50% chemical fertilizer (150 kg/ha CON2H4, 50 kg/ha Na3PO4, and 50 kg/ha KCl) + 1 ton/ha SF, and CFSF2 = 50% chemical fertilizer (150 kg/ha CON2H4, 50 kg/ha Na3PO4, and 50 kg/ha KCl) + 2 ton/ha SF.

3.1. Effect of SF Supplementation on Rice Plant Growth Field Scale

After 110 days of planting, the rice plants were harvested. This harvest time was based on the recommendation of days to harvest (DTH) for the Inpari 32 rice strain, which is approximately 110 days [23]. Based on the rice plant growth observation, the groups with SF supplementation showed faster maturation time compared to the CF group (Figure 2A–C). The change in color of the paddy rice panicles from green to brown indicates the maturation of grains [24]. In the CF-treated group, the contamination of immature green panicles could still be observed. One reason for a delayed maturation time in plants is due to low soil macronutrient concentrations [25,26]. On the contrary, the rice plants supplemented with SF produced more mature yellowish grains (Figure 2D–F).
Five plant growth hormones have been reportedly found in seaweeds, namely auxins, cytokinins, GAs, ABA, and ethylene [27]. The ethylene presence in seaweeds possibly explains the accelerated maturation of the rice plants with SF applied. These hormones also have a significant effect during tiller bud growth of grains to rice [28]. Furthermore, based on the rice plant’s physical size, there were significant differences in the height of SF-supplemented rice plants (Figure 2G). The height of rice plants supplemented with a normal CF dose showed similar results to other studies which also used the same rice variant, inpari32 [29]. Increased concentrations of SF supplementation showed increased plant height up to 87.01 ± 1.43 cm. Plant height is an important trait for rice plants, if the plant is too short, it will produce fewer grains. In addition, if the plant is too high, it will have poor lodging resistance. Furthermore, SF supplementation was also seen to significantly increase tiller numbers (Figure 2H). The tiller number of rice plants plays an important role for panicle architecture, and thus significantly affects the number of grains produced [30]. The number of tillers produced in SF-supplemented rice plants significantly increased to 20–25 tillers per plant. This is significantly higher compared to the rice plants treated with only chemical fertilizer (15.33 ± 1.15 tillers/plant). The number of tillers has been reported to positively contribute to achieving high yield grains in rice [31,32]. This possibly explains the significantly higher number of grains formed in rice plants treated with SF supplementation (Figure 2I).
The use of seaweed as a fertilizer should take into account the formulation and application method. Our current results show that seaweed-based fertilizers are best used in combination with a reduced concentration of inorganic fertilizers (reduced up to approximately 50% the normal dose). The use of seaweed-based fertilizers alone has not proven to be efficient for plant growth. This is also in line with other studies showing a negative effect of seaweed-based fertilizer usage on plant growth [33]. Even so, there are also other studies that show the fertilizer potential of the brown seaweed Sargassum spp. [34].

3.2. Soil Chemical Properties

Macronutrient composition of soil growth medium after harvest was investigated (Table 3). All main soil macronutrients, nitrogen (N), phosphorus (P), and potassium (K), remained significantly high in soil supplemented with SF. Based on previous studies, organic fertilizers commonly increased the N, P, and K levels in soils [35,36]. Similar results were also seen in seaweed-based organic fertilizers [37,38]. The sufficient concentration of NPK in SF-treated soils indicate the soil fertility status. The levels of NPK in SF-treated soils remained adequate even after harvest. Sufficient amounts of the primary soil macronutrients would benefit the next plantation, which could potentially further reduce the use of chemical fertilizers. Agricultural croplands with the highest N concentration would produce some of the highest crop yields [39].
Supplementation of SF in soil significantly affects nitrogen (N) concentration, which affects almost all levels of plant function including growth and development [36]. Although soil P receives limited attention compared to N, it still should be considered as one of the crucial macronutrients for supporting plant growth [40]. Low soil P concentration is a limiting factor for plant growth and health [41]. The supplementation of SF was also seen to significantly increase K levels in soil. Potassium is also a crucial macronutrient which plays a role in plant growth and development [42]. In addition, seaweeds have been reported to contain high potassium content [37].
The increase in the soil macronutrients N, P, and K after seaweed fertilizer treatment has also been reported in other studies [43,44]. Seaweed fertilizer treatment may contribute to the increase of microbial population in the soil [12,13]. In addition, short-term application of seaweed fertilizer has shown significant changes in soil microbial communities [45]. The microbial community associated with seaweed contains a diverse assembly of various microorganisms, including bacteria, archaea, and also fungi. Collectively, these associated microorganisms are known as “seaweed holobiont” [46]. Therefore, these microorganisms may contribute to the robust growth of certain seaweeds, such as the brown seaweeds Sargassum spp. In addition, these microorganisms could be applied to promote the growth of crops by increasing the concentration of nutrients in the soil [47]. Furthermore, various marine microorganisms have been shown to exhibit beneficial properties as plant-growth-promoting bacteria (PGPB) [48].

3.3. Microbial Diversity in SF-Supplemented Soils

The increased macronutrient content in soils treated with SF is presumably due to the change in microbial community. Beneficial microbial interactions could contribute to the improvement of macronutrient availability in the soil [49], whereas the long-term usage of chemical fertilizer has been associated with decreased soil microbial diversity [50]. Hence, composition and diversity of these beneficial soil microbiota are associated with improvement of soil fertility [15]. Therefore, alternative strategies should be considered to reduce the usage of chemical fertilizers in the agricultural system [51].
Based on NGS analyses of treated soil DNA, the treatment groups CF and CFSF1 showed similar microbial abundance (Figure 3). A distinct microbial profile was only observed in the CFSF2 group which had a higher concentration of SF applied (2 ton/ha). Notably, there is a large portion of the Archaea phylum Crenarchaeota in the CFSF2 group. The phylum Crenarchaeota is most commonly abundant in marine environments [52]. However, there are some novel Crenarchaeota found in forest and also paddy soil [53,54]. Hence, we could not confirm the origin of the presence of this Archaea in the CFSF2 group.
The Crenarchaeota phylum is also referred to as ammonia-oxidizing archaea (AOA), which are important players in the nitrogen cycle [55]. Ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) play a crucial role in the oxidation of ammonia, which is particularly important for soil fertility [56]. The macronutrient N is essential to supporting plant growth. The availability of this macronutrient is largely due to the aerobic oxidation of ammonia to nitrate. Hence, the microbes which are involved in this process provide valuable ecological services in the agricultural system [57].

3.4. Microbial Functional Prediction in SF-Supplemented Soils

In addition to microbial community and diversity analyses, the potential bacterial functional genes were also evaluated. The prediction of functional genes has been shown to provide an essential link between microbial diversity patterns and ecosystem function [58]. A previous study has also shown that the addition of seaweed fertilizer improved beneficial enzymes such as urease and dehydrogenase [59]. The functional composition of sampled microbial communities can be evaluated with the PICRUSt tool [20]. PICRUSt was first developed and introduced in 2013 to predict the function of observed microbial community based on its metagenome 16S profile [20,21]. The generated OTU table was imported into the PICRUSt software version 1.1.4 which predicted the functional gene and protein content of the various microbial communities based on the Kyoto Encyclopaedia of Genes and Genomes (KEGG), BioCyc, and PFAM databases to predict the functional gene and protein content of the various microbial communities in SF-supplemented soils [60,61,62,63]. Based on the different annotation databases observed, the CFSF2 group is mostly enriched by genes which function for amino acid metabolism (Figure 4A–C). However, this pattern is most obvious in the KEGG and BioCyc pathway functional annotation databases. This presumably supports our previous findings that SF supplementation increases amino acid content in rice plants [13]. In addition, the genes related to nucleotide metabolism, such as Phosphoribosylformylglycinamidine synthetase (or PFAS), were also increased in the CFSF2 treatment group. This is a highly conserved enzyme which is involved in the fourth step of de novo purine synthesis [64]. Purines are essential for various cellular processes, including DNA replication, transcription, and energy metabolism [65]. Other than amino acid metabolism, the CFSF2 group also showed enrichment of functional genes related to carbohydrate metabolism. Including transketolase, this enzyme is a key enzyme in the pentose phosphate pathway which catalyzes the formation of various sugar phosphates [66]. Another important enzyme for carbohydrate metabolism is UDP-glucose-4-epimerase (UGE); this enzyme has been found to be N-responsive and expressed in an N-dependent manner [67]. In comparison to the CFSF2 group, the CF and CFSF1 groups were more abundant in functional genes related to signaling and cellular processes. However, one functional gene related to amino acid metabolism was seen to be enriched in the CFSF1 group: glutamine synthetase. Glutamine synthetase is required for glutamine (Gln) synthesis, which is an amino acid necessary for nitrogen (N) assimilation in plants [68]. There were two genes enriched in the CF group which play an important role in fatty acid biosynthesis [69]. Fatty acid content is considered as one of the key metabolites which correlates to rice storage [70]. There have been some reports that organically grown rice would be more likely to be contaminated with mycotoxin-producing fungi [71]. Hence, further research is needed to confirm the shelf time of rice produced with SF supplementation.
Furthermore, based on the PFAM database, two protein families were increased in the CFSF2 group which were related to amino acid metabolism: the aminotransferase class I/II and pyridoxal-phosphate-dependent enzyme (PLP). The Aminotransferase protein family catalyzes the reaction of nitrogen in amino acids in both protein metabolism and gluconeogenesis [72]. Aminotransferase class I/II is a subgroup of aminotransferases which includes aspartate aminotransferase, aromatic amino acid aminotransferase, alanine transferase, and histidinol phosphate aminotransferase [73]. Aspartate is an essential metabolite required for plant growth, particularly during vegetative growth [74]. The aromatic amino acid group members such as phenylalanine, tyrosine, and tryptophan are essential amino acids for protein synthesis and also precursors for a wide range of secondary metabolites [75]. Pyridoxal-phosphate-dependent enzyme (PLP) plays an important role in metabolic roles for nitrogen metabolism [76]. In addition, PLP–dependent enzymes are mostly involved in the regulation of amino acid biosynthesis [77]. In addition, critical steps of tryptophan (Trp) metabolism and synthesis are regulated by PLP-dependent enzymes [78]. Essential amino acids such as Trp have been reported to increase the ability of plant cells in water and nutrient uptake from the soil [79]. Sufficient water and nutrient uptake are necessary to sustain plant growth and development, especially in rice plants which require high amounts of water [80,81]. In contrast, the CF group showed enrichment of proteins involved in genetic information processing and cellular signaling processes. In addition, a protein involved in fatty acid metabolism was also observed in the CF group, Enoyl-(Acyl carrier protein) reductase. This protein, also known as ENR, catalyzes the final step of bacterial fatty acid elongation [82].

3.5. Unique Operational Taxonomical Units (OTUs) in SF-Supplemented Soil

Analyses with Venn diagrams show compartmental core microbiota OTU distributions in SF-treated soil based on the Kyoto Encyclopaedia of Genes and Genomes (KEGG), BioCyc, and PFAM databases (Figure 5A–C) based on Venn diagram visualization of KEGG pathways, where CFSF2 resulted in the highest unique pathways, followed by CF and CFSF1. In addition, approximately 7806 shared KEGG gene annotations were shared among the three treatments. However, based on BioCyc gene annotations, there were 407 core metabolic pathways shared between the treatments. The number of unique pathways was significantly lower compared to the gene annotations in the KEGG database. This is possibly due to the fact that the KEGG pathway database is 4.2 times larger compared to the BioCyc pathway database [83]. Furthermore, the number of unique PFAM domains in CFSF2 was higher compared to CFSF1 and CF. In addition, CFSF1 actually had lower PFAM-unique domains compared to CF. There were approximately 6866 PFAM domains shared between the three treatments. The shared functional genes between the treatments possibly indicate the functional genes which are involved in core metabolic pathways [84]. Hence, it could be assumed that SF supplementation increased the enrichment of various functional genes and pathways.
Another study also showed functional changes of soil bacteria which enhance crop productivity and stress tolerance. However, this study was conducted with the commercial red seaweed Kappaphycus alvarezii [85]. The current study describes the effects of the non-commercial brown seaweed Sargassum spp. on the soil microbial functional genes. The brown seaweed Sargassum spp. is currently a wild seaweed and considered a pest and marine debris to the commercial seaweed K. alvarezii. Hence, bioprospecting of the brown seaweed Sargassum spp. would not only contribute to agricultural productivity but also the seaweed aquaculture industry (Figure 6).

4. Conclusions

Excessive use of chemical fertilizer degrades soil fertility and macronutrient content, which are essential for plant growth and development. Supplementation of SF in soil of rice plants was seen to improve macronutrient composition. In addition, the increased concentration of SF in CFSF2 showed a significant increase in Archaea Crenarchaeota, which plays a crucial role in nitrogen cycling. Hence, the presence of this Archaea in the CFSF2-treated soil is potentially associated with maintaining soil fertility. Furthermore, SF supplementation increases the enrichment of functional genes and protein domains related to amino acid, nucleotide, protein, and carbohydrate metabolism. However, isolation of the beneficial bacteria in SF-supplemented soil would be essential for the further utilization of valuable bacterial metabolites or enzymes in agricultural systems. In conclusion, the bioprospecting of the wild brown seaweed Sargassum spp. as fertilizer for crop production has a potential dual effect on both sustainable agricultural and aquaculture systems.

Author Contributions

E.S.P. was responsible for funding acquisition, research conceptualization, methodology, validation, formal analysis, and writing—original draft; N.S.H.K. contributed to the methodology and investigation; F.F. and P.B.A.S. contributed to the formal analyses; W.Q. contributed to the investigation; B.T.K.I. was responsible for supervision and project administration; A.H. contributed to formal analyses and responsible for software and visualization; and S.W. was responsible for supervision and review of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Research Funding from the Indonesian Ministry of Education, Culture, Research and Technology (KEMENDIKBUD-DIKTI) under applied research (PTK) grant no. 2351/UN18.L1/PP/2023.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data that support the findings of this study are available from the corresponding author.

Acknowledgments

All the authors acknowledge the technicians and lab staff of the Bioscience and Biotechnology Research Center (Pusat Unggulan Iptek Biosains dan Bioteknologi) University of Mataram that have supported this research.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Experimental model field layout of rice crop for each fertilizer treatment. The water irrigation area is depicted as the grey area. Each experimental plot is 0.02 ha (2 ares) wide.
Figure 1. Experimental model field layout of rice crop for each fertilizer treatment. The water irrigation area is depicted as the grey area. Each experimental plot is 0.02 ha (2 ares) wide.
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Figure 2. Evaluation of effects of SF supplementation on rice plant productivity. Morphological features of rice plants treated with (A) only chemical fertilizer (CF), (B) 50% CF + 1 ton/ha SF (CFSF1), and (C) 50% CF + 2 ton/ha SF (CFSF2). Measurement of grains produced from rice plants supplemented with (D) CF, (E) CFSF1, and (F) CFSF2. Effects of SF on rice plant (G) height, (H) tiller number, and (I) grain weight. Results are the mean ± SEM of three separate experiments. * p < 0.05 between treatments. ** p < 0.01 between treatments. ns indicates no significant differences between treatments.
Figure 2. Evaluation of effects of SF supplementation on rice plant productivity. Morphological features of rice plants treated with (A) only chemical fertilizer (CF), (B) 50% CF + 1 ton/ha SF (CFSF1), and (C) 50% CF + 2 ton/ha SF (CFSF2). Measurement of grains produced from rice plants supplemented with (D) CF, (E) CFSF1, and (F) CFSF2. Effects of SF on rice plant (G) height, (H) tiller number, and (I) grain weight. Results are the mean ± SEM of three separate experiments. * p < 0.05 between treatments. ** p < 0.01 between treatments. ns indicates no significant differences between treatments.
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Figure 3. Taxonomic profiles of the microbial populations observed in the soil of the three different treatments, CF, CFSF1, and CFSF2. Microbial composition observed by the ASV pipeline is shown in the legend provided on the right of the scale bar.
Figure 3. Taxonomic profiles of the microbial populations observed in the soil of the three different treatments, CF, CFSF1, and CFSF2. Microbial composition observed by the ASV pipeline is shown in the legend provided on the right of the scale bar.
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Figure 4. Functional annotations predicted by PICRUSt based on (A) KEGG, (B) BioCyc, and (C) PFAM pathway databases of the soil microbiome communities.
Figure 4. Functional annotations predicted by PICRUSt based on (A) KEGG, (B) BioCyc, and (C) PFAM pathway databases of the soil microbiome communities.
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Figure 5. Venn diagram showing (A) KEGG, (B) BioCyc, and (C) PFAM database pathway protein domain enrichment in soils supplemented with SF.
Figure 5. Venn diagram showing (A) KEGG, (B) BioCyc, and (C) PFAM database pathway protein domain enrichment in soils supplemented with SF.
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Figure 6. Illustration of sustainable potential of seaweed fertilizer in agricultural crop systems.
Figure 6. Illustration of sustainable potential of seaweed fertilizer in agricultural crop systems.
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Table 1. Physiochemical properties of soil in experimental field.
Table 1. Physiochemical properties of soil in experimental field.
Physical PropertiesChemical Properties (g/kg)
pHTextureTotal N Total PTotal K
7.63 ± 0.17Sandy2.13 ± 0.150.54 ± 0.030.83 ± 0.02
Table 2. Fertilizer treatments that were applied at each test site. All measurements are in kg/ha.
Table 2. Fertilizer treatments that were applied at each test site. All measurements are in kg/ha.
Treatment Group NameInorganic FertilizerSeaweed Based Organic Fertilizer
CON2H4Na3PO4KCl
CF300100100-
CFSF115050501000
CFSF215050502000
Table 3. Macronutrient properties of soil treated with seaweed-based fertilizer.
Table 3. Macronutrient properties of soil treated with seaweed-based fertilizer.
TreatmentTotal N (g/kg)Total P (g/kg)Total K (g/kg)
Before fertilization2.13 ± 0.15 a0.34 ± 0.03 a0.43 ± 0.02 a
CF1.18 ± 0.15 b0.23 ± 0.01 a0.48 ± 0.03 a
CFSF12.67 ± 0.15 c0.61 ± 0.03 b0.97 ± 0.03 b
CFSF22.77 ± 0.12 c0.60 ± 0.02 b1.07 ± 0.01 b
Different superscript letters indicate significant differences (p < 0.05) between treatments within one column.
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Prasedya, E.S.; Kurniawan, N.S.H.; Fitriani, F.; Saraswati, P.B.A.; Qoriasmadillah, W.; Ilhami, B.T.K.; Hernawan, A.; Widyastuti, S. Sustainable Use of Organic Seaweed Fertilizer Improves the Metagenomic Function of Microbial Communities in the Soil of Rice Plants. Sustainability 2023, 15, 16328. https://doi.org/10.3390/su152316328

AMA Style

Prasedya ES, Kurniawan NSH, Fitriani F, Saraswati PBA, Qoriasmadillah W, Ilhami BTK, Hernawan A, Widyastuti S. Sustainable Use of Organic Seaweed Fertilizer Improves the Metagenomic Function of Microbial Communities in the Soil of Rice Plants. Sustainability. 2023; 15(23):16328. https://doi.org/10.3390/su152316328

Chicago/Turabian Style

Prasedya, Eka Sunarwidhi, Nanda Sofian Hadi Kurniawan, Fitriani Fitriani, Putu Bella Aprillia Saraswati, Wanda Qoriasmadillah, Bq Tri Khairina Ilhami, Ari Hernawan, and Sri Widyastuti. 2023. "Sustainable Use of Organic Seaweed Fertilizer Improves the Metagenomic Function of Microbial Communities in the Soil of Rice Plants" Sustainability 15, no. 23: 16328. https://doi.org/10.3390/su152316328

APA Style

Prasedya, E. S., Kurniawan, N. S. H., Fitriani, F., Saraswati, P. B. A., Qoriasmadillah, W., Ilhami, B. T. K., Hernawan, A., & Widyastuti, S. (2023). Sustainable Use of Organic Seaweed Fertilizer Improves the Metagenomic Function of Microbial Communities in the Soil of Rice Plants. Sustainability, 15(23), 16328. https://doi.org/10.3390/su152316328

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