Microbial diversity and biotechnological potential of mangrove leaf litter in Kebun Raya Mangrove, Surabaya, Indonesia

Diversidade microbiana e potencial biotecnológico da serrapilheira de mangue em Kebun Raya Mangrove, Surabaya, Indonésia

Abstract

Mangrove ecosystems play a crucial role in maintaining ecological balance with leaf litter serving as an important substrate for diverse microbial communities. This study investigates the microbial communities inhabiting leaf litter from four different mangrove species: Rhizophora apiculata, Rhizophora stylosa, Sonneratia caseolaris, and Avicennia marina collected from Kebun Raya Mangrove, Surabaya, Indonesia. Using metagenomic sequencing, we revealed that Proteobacteria were predominant, followed by Chlorobi and Actinobacteria in the samples. Interestingly, we detected notable populations of anaerobic bacteria, including genus of Chlorobaculum and Allochromatium. Metagenomic analyses exhibited high levels of adaptation to stressors, evidenced by the prevalence of genes conferring resistance to antibiotics (e.g., beta-lactams, tetracyclines), heavy metals (e.g., chromium, arsenic), and hydrocarbons. Furthermore, the metagenomic analysis revealed the presence of genes involved in the biosynthesis of polyunsaturated fatty acids (PUFAs), antimicrobial compounds, and plant growth-promoting activities. These findings highlight the potential of mangrove leaf litter as a reservoir of beneficial microbes with diverse biotechnological applications, including bioremediation, nutraceuticals, pharmaceuticals, and agriculture.

Keywords:
microbiome; mangrove leaf litter; metagenome; biodiversity; biotechnological potential

Resumo

Os ecossistemas de manguezais desempenham um papel crucial na manutenção do equilíbrio ecológico, com a serrapilheira servindo como um substrato importante para diversas comunidades microbianas. Este estudo investiga as comunidades microbianas que habitam a serrapilheira de quatro diferentes espécies de manguezais: Rhizophora apiculata, Rhizophora stylosa, Sonneratia caseolaris e Avicennia marina, coletadas em Kebun Raya Mangrove, Surabaya, Indonésia. Utilizando sequenciamento metagenômico, revelamos que as Proteobacterias foram predominantes, seguidas por Chlorobi e Actinobacteria nas amostras. Detectamos populações notáveis de bactérias anaeróbias, incluindo espécies de Chlorobaculum e Allochromatium. As análises metagenômicas exibiram altos níveis de adaptação a estressores, evidenciados pela prevalência de genes que conferem resistência a antibióticos (por exemplo, betalactâmicos, tetraciclinas), metais pesados (por exemplo, cromo, arsênio) e hidrocarbonetos. Além disso, a análise metagenômica revelou a presença de genes envolvidos na biossíntese de ácidos graxos poli-insaturados (PUFAs), compostos antimicrobianos e atividades de promotoras do crescimento das plantas. Essas descobertas destacam o potencial da serrapilheira de manguezal como um reservatório de micróbios benéficos com diversas aplicações biotecnológicas, incluindo biorremediação, nutracêuticos, produtos farmacêuticos e agricultura.

Palavras-chave:
microbioma; serrapilheira de manguezal; metagenoma; biodiversidade; potencial biotecnológico

1. Introduction

Indonesia has the largest mangrove forest in the world with total area approximately 28 km² (Jia et al. 2023). Mangrove ecosystems are crucial for coastal protection, biodiversity and ecological conservation and sustainability. Leaf litter is one part of the mangrove ecosystems which serves important roles in organic matter decomposition, nutrient cycling, and ecosystem resilience. These biogeochemical processes make the mangrove leaf litter is a vital substrate for microbial colonization responsible for the processes.

The high availability of organic matter is directly related to the abundance of mangrove microorganisms (Mamidala et al., 2023). The abundance of microorganisms in the environment, known as the mangrove microbiome, consists of bacteria and fungi, algae, and protozoa (Palit et al. 2022). The abundance of organic matter in mangrove ecosystems triggers the abundance of detritus microorganisms(Sukmawati et al. 2022). Detritus microorganisms play a role in nutrient cycling in mangroves, including decomposing litter that falls on mangrove sediments (Islam et al., 2024). During the lengthy decomposition process of litter, microbes play a crucial role, especially in the initial stages of leaching dissolved organic matter, which leads to the release of organic carbon, nitrogen, and polyphenols (Pradisty et al., 2021). Bacteria groups like Azotobacter sp. and fungi groups like Ascomycota have been shown to secrete important exudates and enzymes that aid in this decomposition process (Palit et al., 2022). The importance of microbes in nutrient cycling in mangrove ecosystems demonstrates their potential as biofertilizer agents(Thatoi et al., 2020).

As it located in estuarine area, the microbial communities are continuously exposed to stressors coming form anthropogenic activities in the form of urban runoff that carries pollutants as well as nutritions. The mangrove area in Indonesia, particularly Kebun Raya Mangrove, Surabaya currently has significant records of plastic waste and pollutant contamination due to anthropogenic activities from urban and industrial areas, such as industrial and household waste disposal in the Wonorejo River (Titah and Pratikno, 2020). The pollution of the Wonorejo River directly impacts the coastal mangrove ecosystem due to tidal fluctuations in the Madura Strait (Trimulono et al., 2022). Coastal pollution can make the mangrove environment extreme for indigenous microorganisms because it are often exposed to contaminants and pollutants(Wang and Gu, 2021).

Mangrove microbial communities are generally known for their adaptive capabilities to environmental stress(Pradisty et al., 2021). Mangrove microbes can tolerate environmental stress through unique cellular metabolic pathways, such as microbial oxidation and reduction processes with mangrove roots to degrade or detoxify contaminants(Palacios et al., 2021). Several studies have shown that mangrove microbes possess stress-tolerant genes (salinity and contaminants) that can produce enzymes and proteins with potential for biotechnology development, such as bioremediation efforts(Sepulveda-Correa et al., 2021). Furthermore, mangrove microbial communities are known to produce new bioactive compounds due to the high diversity of Actinobacteria(Andreote et al., 2012). Actinobacteria groups can produce various antibacterial compounds, such as non-ribosomal peptides (NRPS), which control multi-drug-resistant bacteria, showing potential as antitumor, antioxidant, and antimicrobial agents(Sepulveda-Correa et al., 2021).

Here we investigated the microbial community profiles of mangrove leaf litter collected from 4 different species inhabiting Kebun Raya Mangrove Surabaya, Indonesia as well as exploring the abundance of biotechnologically important genes related to the resistance against various stressors, and functional genes in the field of nutraceutical, pharmaceutical and agriculture.

2. Materials and Methods

2.1. Sample collection and environmental parameters measurement

Leaf litter were collected from 4 different species: Rhizopora apiculata, Rhizospora stylosa, Sonneratia caseolaris, and Avicennia marina. The location of collection was at Kebun Raya Mangrove Surabaya (Table 1, Figure 1). We collected leaf litter using composite sampling method by taking several leaves of the mangrove found in the water surrounding the mangrove tree in three different spots. We also measured the temperature and pH of the water using pH meter and salinity of the water using refractometer from 3 different spots of each corresponding sampling area. We conducted the sample collected and environmental parameters measurement from 2 individuals for each species.

Table 1
Sampling location.

Sample code	Species	Location based on GPS
RA1	Rhizopora apiculata	Lat -7.308718; Long 112.822132
RA2		Lat -7.308832; Long 112.82189
RS1	Rhizopora stylosa	Lat -7.292283; Long 112.813344
RS2		Lat -7.308663; Long 112.821706
SC1	Sonneratia caseolaris	Lat -7.292833; Long 112.814834
SC2		Lat -7.308663; Long 112.821706
AM1	Avicennia marina	Lat -7.308832; Long 112.82189
AM2		Lat -7.307736; Long 112.82184

Figure 1
Sampling location at Kebun Raya Mangrove Surabaya, Indonesia. The map was created using GPSVisualizer.com (Schneider, 2023).

2.2. DNA extraction

The collected leaf litter samples were then soaked in sterile water containing 0.9% NaCl and agitated at 150 rpm for 2 h. The supernatants were then subjected to DNA extraction using Zymbiomic DNA Miniprep kit (Zymo Research).

2.3. Metagenomic analysis

2.3.1. Library preparation and sequencing

The extracted DNA were then quality controlled and randomly fragmented using Covaris technology. The fragments were then used for library construction and sequenced using the DNBSeq platform. High quality reads were then assembled using MEGAHIT (Li et al., 2015). The obtained sequence were subjected to bioinformatic analysis, statistic analysis and deposited to NCBI with bioproject ID PRJNA1105732.

2.3.2. Taxonomic and functional analysis

The obtained reads were functionally annotated using DIAMOND (Buchfink et al., 2015) BLASTP search against databases namely BacMet, an antibacterial biocide and metal resistance genes database (Pal et al., 2014), Card, a comprehensive antibiotic resistance database (Jia et al., 2017), KEGG, genes and genomes database (Ogata et al., 1999), eggNOG, a public database of orthology relationships, gene evolutionary histories and functional annotations (Huerta-Cepas et al., 2019), COG, cluster of orthologoue genes database (Galperin et al., 2015), SwissProt, a curated protein database (Poux et al., 2017), and CAZy, a database about enzymes involved in the synthesis, metabolism, and recognition of complex carbohydrates (Lombard et al., 2014). The obtained predicted gene functions were then used to analyze the readcount relative abundance of the gene of interest (Luqman et al., 2020). To analyse the diversity in the samples, we calculated Shannon-Wiener index, Chao1 index and Simpson index which quantifies the the overall number of species within each sample and their frequency of occurrence. The obtained species data from each sample were then further analysed for principle component analysis and heatmap similarity clustering.

2.4. Statistical analysis

Data distribution of the diversity indexes and physicochemical parameters were analysed using Saphiro-Wilk test. The results of this data distribution test were used to determine the correlation test. The normally distributed data were further analysed using Pearson’s correlation test while not normally distributed data were analysed using Spearman’s correlation test.

3. Results

3.1. Mangrove leaf litter were predominantly inhabited by bacteria

Leaf litter collected from 4 mangrove species were inhabited by various microorganisms with more than 99% are from domain bacteria. Viral DNA was also shown to be detected in the leaf litter collected from S. caseolaris and A. marina from 2 different locations were relatively more abundant compared to the other samples (Figure 2A). In the phylum level, Proteobacteria generally was found to be dominant in all samples followed by Chlorobi or Actinobacteria (Figure 2B). In the family level, leaf litter collected from R. apiculata showed different composition pattern between 2 samples, Vibrionaceae followed by Rhodobacteriaceae were dominant in RA1 while in RA2, Chlorobiaceae was found to be predominant. Whereas, for leaf litter collected from R. stylosa shown similar pattern in both samples with Rhodobacteriaceae is dominant. Enterobacteriaceae and Pseudomonadaceae were found to be predominant in samples from S. caseolaris and A. marina (Figure 2C). In genus level, Vibrio appears to be predominant in all samples except in RA2 that has Chlorobaculum to be the dominant one. Interestingly, there are some species from anaerobic bacteria that were quite dominant in the samples, such as Chlorobaculum parvum, Chlorobaculum tepidum, Chlorobaculum limnaeum, Allochromatium vinosum, Prosthecochloris sp. and Thiocystis violascens (Figure 2D).

Figure 2
Microbiome abundance in taxa level from leaf litter of four Mangrove species: (A) Domain, (B) Phylum, (C) Family, and (D) Species.

3.2. Leaf litter from the same species can have different microbiota composition

We further analysed the metagenomic data using the identified microbiota species in each samples using PCoA analysis and then clustered the samples based on the microbial communities similarity. It turned out that leaf litter collected from RS1 and RS2 showed high similarity to each other as well as SC1 and SC2. However, leaf litter from AM1, AM2 and RA1 and RA2 showed relatively different pattern as depicted in Figure 3. This suggests that the microbiota diversity in leaf litter is not only defined by the species of the host.

Figure 3
Similarity of microbial communities found on mangrove leaf litter. The microbial communities were analyzed at the species level to investigate the similarity between samples and species usiang (A) Principle Component Analysis and (B) heatmap similarity clustering.

As we collected mangrove leaf litter from different locations, we also measured the environmental parameters, such as pH, temperature and salinity. The obtained pH value was still in a neutral range between 7 – 7.8. The measured temperature of the substrate where the leaf litter was collected was ranged between 31.7 – 34 ºC and the salinity values were categorized as brackish (0.6 – 1.6%) (Table 2). The diversity analyses using Shannon, Simpson and Chao1 index show that microbial communities in all samples have relatively similar diversity level (Table 2). Statistical analyses show that the species richness, represented by Chao1 index, was negatively correlated with the pH and salinity (P-value < 0.05) (Table 3).

Table 2
Alpha diversity of microorganisms detected in each sample.

Sample code	Species	Physicochemical parameters			Diversity indexes
		pH	Temperature (ºC)	Salinity (%)	Shannon	Simpson	Chao1
RA1	Rhizopora apiculata	7.8	33.2	1	4.94	0.89	5254
RA2		7.4	34	1	5.27	0.94	5175
RS1	Rhizopora stylosa	7	33.3	1.3	6.63	0.99	5114
RS2		7.4	32.8	1	6.67	0.99	5176
SC1	Sonneratia caseolaris	7.2	31.7	1.4	5.62	0.98	5041
SC2		7.5	31.8	1.6	5.68	0.98	4935
AM1	Avicennia marina	7.3	32.1	0.6	6.55	0.99	5092
AM2		7.3	33.7	1	6.03	0.98	5284

Table 3
Statistical analyses of physicochemical parameters and diversity indexes.

Diversity Index	Physicochemical Parameter	Data Distribution	Correlation Method	Correlation Coefficient	p-Value
Shannon	pH	Normal	Pearson	0.30	0.46
Shannon	Temperature	Normal	Pearson	-0.11	0.81
Shannon	Salinity	Normal	Pearson	0.02	0.97
Simpson	pH	Non-Normal	Spearman	0.37	0.36
Simpson	Temperature	Non-Normal	Spearman	0.00	1.00
Simpson	Salinity	Non-Normal	Spearman	0.02	0.96
Chao1	pH	Normal	Pearson	-0.72	0.04
Chao1	Temperature	Normal	Pearson	0.60	0.12
Chao1	Salinity	Normal	Pearson	-0.72	0.04

3.3. Resistance genes against various stressors were prevalent in mangrove leaf litter

As estuarine area is constantly exposed to the stressors from urban runoff. It is interesting to see the adaptation of the microbial community in the mangrove leaf litter against various pollutants, such as antibiotics, heavy metals and hydrocarbons/plastic. The relative read of genes based on the gene’s read was analyzed from the metagenome data to obtain an overview of the presence of the resistance genes. We found that in mangrove leaf litter, the microbial community possess the genes to tollerate the pollutants exposure. One example is the antibiotic stressors, the relative read number of the resistance genes against beta lactam antibiotics, such as penicillin and against tetracycline are particularly high. We also observed other resistance genes against vancomycin, kanamycin, fluoroquinolone, and erythromycin (Figure 4A). For resistance against heavy metal exposure, the resistance genes against chromium (Cr), arsenic (As), and iron (Fe) are relatively higher. It is understandable that genes related to the tollerance or utilization of Fe are prevalent since Fe is a micronutrient crucial for organisms including microbes (Figure 4B). Another interesting resistance genes found are against hydrocarbon and plastic, as it is known that plastic are found contaminating anyplace. We observed that the microbial community in mangrove leaf litter harbor the capability to degrade hydrocarbons as represented by the presence of hydrocarbon degrading genes in the samples. Besides, although not so prevalent, it is exhibited that the samples contain cutinase-encoding gene, a plastic degrading enzyme, which suggests that microbes inhabiting mangrove leaf litter have a potential to be utilized and exploited to degrade plastic (Figure 4C).

Figure 4
Micorbiome of mangrove leaf litter harbors resistance genes against stressors. Heatmap of the relative reads of (A) antibiotic resistance genes, (B) heavy metal resistance genes, and (C) hydrocarbons or plastic degrading genes. Small subunit ribosomal (house keeping gene) is used as a comparison.

3.4. Potential genes for microbes exploitation in mangrove leaf litter

Many studies isolated the beneficial microbes that possess the particular ability to be potentially exploited. Therefore, we investigated the abundance of the beneficial genes from the mangrove leaf litter samples, such as genes related to PUFA production, antimicrobial production, and plant growth-promoting activities. In terms of PUFA production, fadL, a genes encodes a long chain fatty acids importer (Salvador Lopez and Van Bogaert, 2021) and fadC gene that encodes acy-CoA synthetase that catalyses the activation of imported long chain fatty acids (LCFA) into acyl-CoAs (Santos-Merino et al., 2018) were found to be relatively abundant across the samples. Interestingly, FADS1 gene that encodes a desaturase that play a pivotal role in arachidonic acid (AA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) biosynthesis (Ralston et al., 2015) was found to be abundant in leaf litter collected from S. caseolaris (SC1 and SC2) and R. apiculata (RA1) (Figure 5A).

Figure 5
Microbial community in mangrove leaf litter posses potential genes. Heatmap of the relative reads of (A) PUFA biosynthesis genes, (B) antimicrobial biosynthesis genes, and (C) biofertilizer activity-related genes. Small subunit ribosomal (house keeping gene) is used as a comparison.

We also observed the high abundance of Microcin C transport-related genes across the samples which might indicate the possibility of the presence of Microcin biosynthesis-related genes but at low read number. Interestingly, despite the low abundance, the genes related to lantibiotic biosynthesis was present across the samples, which suggests the potential of further exploitation on putatively novel lantibiotics from microbial communities inhabiting mangrove leaf litter (Figure 5B). Another important potential of mangrove leaf litter is as a source of biofertilizer. The analyses from metagenome data from the collected leaf litter shown that the samples harbor a fast biofertilizer-related activities, such as nitrogen fixation and metabolism, phosphate, potassium and sulfur metabolisms, stress tollerance, symbiosis support, antifungal, iron acquisition, and plant hormones production to enhance plant’s growth across all the samples with relatively high abundance (Figure 5C).

4. Discussion

This study shows the microbial composition of the mangrove leaf litter collected from 4 different mangrove species found in Kebun Raya Mangrove, Surabaya, Indonesia and analyze further the potential utilization and exploitation of the microbes inhabiting the mangrove leaf litter using NGS technology. Based on the microbiome profiling, more than 99% of the microorganisms detected belong to the domain Bacteria followed by Archaea and Eukaryota. In the genus level, we found that Vibrio was predominant in some samples due to their capability to utilize particulate and dissolved organic matter, even to degrade hydrocarbons and also to reduce nitrate which gives this genera an advantage in anoxic habitat such as mangrove leaf litter, an organic rich substrate (Grimes et al., 2009; Takemura et al., 2014; Givati et al., 2024). Moreover, the high salinity in the estuarine area as well as the eutrophication caused by urban runoff could cause the increase of Vibrio abundance (Kopprio et al., 2017). Another predominant genera is Chlorobaculum, a green sulfur bacteria, that present probably due to the prolonged hypoxia condition caused by the high organic content in a wetland ecosystem such as mangrove area (Chen et al., 2020; Kumari et al., 2021).

Chlorobaculum was found predominantly in RA2, RS1 and RS2 in which these samples were also found to be clustered due to high similarity in microbial communities profile (Figure 3). These samples are from 2 different species of mangrove, R. apiculata and R. stylosa. It suggests that the microbial communities found in mangrove leaf litter is not directly and not only influenced by the host species but the environmental parameters play a crucial role shaping it. In our study pH and salinity showed to negatively correlated with the diversity of the microorganisms in the mangrove leaf litter. The pH range we obtained was in a neutral ranged between 7 – 7.8 which makes sense that the lower pH showed higher diversity as no acidic pH was recorded from the samples. Similar trend was observed in term of salinity as we recorded the salinity values was between 0.6 – 1.6% which is still categorized as brackish water and no high saline was observed.

Beside the pH and salinity, environmental stressors play an important role in shaping the microbial communities selecting the tolerant microorganisms to raise as predominant in the community. Urban runoff which contains a broad range of contaminants provides a unique condition where the microbial adaptation leads to the selection of microbes that are capable to tolerate the stress. In the case of antibiotic, studies reported that antibiotics has been contaminating water bodies and sediments in Indonesia(Shimizu et al., 2013; Kurniawan and Mariadi, 2019; Pijoh et al., 2021). The exposures of antibiotics as a stressor could increase the spread of antibiotics resistant, which in our study we show that antibiotic resistant genes were highly abundant in the mangrove leaf litter. This is in line with another study using stool samples from Indonesian populations that shows the high prevalence of antibiotic resistant genes which probably due to high consumption of antibiotics (Luqman et al., 2024) that represent the high antropogenic activities related to antibiotics in Indonesia (Muurinen et al., 2022). Interestingly, our study and the study using stool samples from Indonesia populations are in agreement in term of the high abundance of the tetracylcine and beta lactam antibiotics resistant genes (Figure 4A). As these study were conducted in the same region, Surabaya, it might reflect the high usage of tetracycline and beta lactam antibiotics in this region.

Similar tendencies could also be applied in heavy metals and hycrocarbon as stressors in Kebun Raya Mangrove, Surabaya. Heavy metals contamination could lead to the increase of the heavy metal resistome in the environment (Puthusseri et al., 2021; Salam et al., 2023). As many studies reported the heavy metals contamination in this region (Kusmana et al., 2018; Harmesa et al., 2023; Taufiqurrahman et al., 2023; Sari and Purnomo, 2024), it is expected that heavy metals resistant genes are abundant in the samples as shown in Figure 4B. Moreover, this region was also reported to be contaminated by hydrocarbons and plastics (Ilyas et al., 2011; Adyasari et al., 2021; Sari et al., 2021; Sari et al., 2022). These contaminations drive the selection of the tolerant microorganisms or even microorganisms with capability to degrade hydrocarbons and plastics as shown in Figure 4C, the genes related to hydrocarbons and plastic degradation were present in the samples. This result was in agreement with many studies regarding the presence of hydrocarbon and plastic degradation genes in the contaminated environment (Liu et al., 2015; Ehis-Eriakha et al., 2020; Das et al., 2022; Nugrahapraja et al., 2022; Alami et al., 2023; Kuswytasari et al., 2023). The ability to degrade contaminant possessed by the microbes present in this ecosystem could be exploited for human welfare in terms of biodegradation and bioremediation of polluted environments.

Our study shows that the mangrove leaf litter collected from Kebun Raya Mangrove, Surabaya has significant potential not only in terms of biodegradation and bioremediation but also in the field of nutraceutical, pharmaceutical, and agriculture (Figure 5). We observed several potential genes involved in EPA and DHA biosynthesis which is consistent with the findings of several studies that reported some eukaryotes from mangrove ecosystems as PUFA producers (Wang et al., 2019; Abdel-Wahab et al., 2021; Kalidasan et al., 2021; Kua et al., 2024). Furthermore, in the field of pharmaceutical our study shows that the genes involved in microcin C production is relatively abundant which impliess that microcin C-producing microorganisms are present in the samples. This results is in line with other studies that showed antimicrobial-producing microorganisms can be isolated from mangrove ecosystems (Sengupta et al., 2015; Retnowati et al., 2018). Another interesting potential is te utilization of microorganisms from mangrove ecosystems as a source for biofertilizer to increase the growth and productivity of crops. Here, we shows quite a number of genes that are relatively abundant in mangrove leaf litter that are related to enhancement of growth and productivity of crops (Figure 5C), similar to other studies reporting the agriculture potential of microorganisms from mangrove ecosystems (Ravikumar et al., 2004; Behera et al., 2014).

The diverse microbial communities in mangrove leaf litter play crucial role in overall ecosystem health as well as its resilience against environmental stressors. Understanding the potential functional roles of the microbes provides valuable insights into the potential function to be harnessed for significant biotechnological potentials. However, as our study focused on metagenomic analyses, it is important to further investigate using wet lab studies.

5. Conclusion

This study aimed to investigate the microbial communities in mangrove leaf litter collected from the Kebun Raya Mangrove, Surabaya and to explore their potential biotechnological applications. Here we revealed that Proteobacteria dominates the mangrove leaf litter and in the genus level, Vibrio was found to be predominant in general. The microbiome profiles between samples was not only influenced by the species of the host but also environmental parameters, such as pH and salinity. Our study also revealed that mangrove leaf litter has significant potential for biotechnological applications in nutraceuticals, pharmaceuticals, agriculture, and environmental remediation. This potential is supported by the abundance of functional genes associated with resistance to various stressors, including antibiotics, heavy metals, and hydrocarbons, as well as genes related to the production of polyunsaturated fatty acids (PUFAs), antimicrobial compounds, and plant growth-promoting agents.

Acknowledgements

This study was funded by Kementerian Pendidikan, Kebudayaan, Riset, dan Teknologi (074/SPK/D4/PPK.01.APTV/VI/2022).

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Publication Dates

• Publication in this collection
  31 Jan 2025
• Date of issue
  2024

History

• Received
  30 July 2024
• Accepted
  29 Oct 2024