Abstract
Fungi occur in mangroves as saprobes, pathogens, and endophytes of a wide range of timber host substrates and may also be isolated from the water column and bottom sediments. In this study, we explore their biodiversity within a single mangrove forest at Muthupet, Tamil Nadu, India. The study showed a rich diversity of fungi on five decaying host substrates (out of seven host substrates) collected in the intertidal zone, resulting in 78 marine fungal taxa in 67 genera from 11 field collections and 6215 samples. Of the 78 taxa, 56 species (in 47 genera) belong to the Ascomycota and two species (2 genera) to Basidiomycota with the remaining 20 species representing asexual fungi (18 genera). Some fungal species were repeatedly reported: Verruculina enalia (21.65%) was the most frequently collected fungus; Marinosphaera mangrovei (9.2%), Rimora mangrovei (9.15%), Okeanomyces cucullatus (8.7%), Halocryptosphaeria bathurstensis (6%) in the frequent category, Paraconiothyrium cyclothyroides (4.5%), Hysterium rhizophorae (3.5%), Sclerococcum haliotrephum (3.6%), Lulworthia sp. (3.6%), and Farasanispora avicenniae (3%) were infrequently collected. Of the host substrates, Avicennia marina wood pieces harbored 49 fungal species of which 19 were unique. Two-way ANOVA revealed that fungal species richness was not affected irrespective of the collection season (P = 0.239) but was significantly dependent on the wood species (P < 0.001).
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Introduction
Mangroves are tropical and subtropical swampy plants that grow in estuaries, bogs, deltas, and lagoons, and harbor marine fungi in trunks and roots that are permanently or intermittently submerged in water (Kohlmeyer and Kohlmeyer 1979; Hyde and Jones 1988; Hyde and Lee 1995). Mangrove forests are of immense ecological, economic, and of traditional importance (Kathiresan and Bingham 2001). They are considered as the second largest habitat of the Earth’s marine fungal diversity (Jones 2011). Mangroves are the biodiversity hotspots for marine fungi (Shearer et al. 2007). Marine fungi in mangrove environment play a vital role in nutrient recycling by secreting extracellular degradative enzymes (Pointing 1999). The global distribution of marine fungi is understudied in contrast to other microbes, plants, and animals. Schmit and Shearer (2003) reported 625 mangrove fungi of terrestrial, fresh water, and marine origin from 72 mangrove plants distributed across different parts of the world. Marine fungal diversity from east coast of India has been documented by Ravikumar and Vittal (1996), Sarma and Vittal (2000, 2001a), (Sarma et al. (2001), Vittal and Sarma (2006), (Sarma 2016), and (Sridhar 2009), to mention but a few. The species diversity in the west coast of India has been documented by Patil and Borse (1983, 1985), Borse and Hyde (1989), Chinnaraj and Untawale (1992), Chinnaraj (1993), Maria and Sridhar (2003, 2004), Raveendran and Manimohan (2007), Hyde and Sarma (2000), and Sarma and Raghukumar (2013). A comprehensive list of marine fungi from India was provided by Borse et al. (2013, 2018). A total of 17 new higher marine fungi were discovered and documented from India until 2014. The number of new marine fungi has increased significantly as different habitats and substrates are examined for marine fungi (Hyde et al. 2017, 2018). Indian mangroves are vast and support various mangrove trees and salt marsh plants. The Indian mangroves have a total area of around 6749 km2, the fourth largest mangrove area in the world that includes about 59 plant species in 41 genera and 29 families (Naskar and Mandal 1999; Kathiresan and Rajendran 2005; Singh et al. 2012). The east coast of India has the largest mangrove area (80%) in contrast to west coast of India (20%) due to major river deltas of Brahmaputra, Cauvery, Ganges, Godavari, Krishna, and Mahanadi flowing east ward into the Bay of Bengal (Kathiresan and Rajendran 2005). The marine fungi of the Godavari and Krishna deltas have been documented by Sarma and Vittal (2000, 2001a), while the Pichavaram mangroves have been documented by Ravikumar and Vittal (1996) and Sridhar (2009). These studies have shown that in spite of their proximity, 50% of the fungal species found were different at each location with few overlapping species. Mangrove fungal diversity has been studied intensively from a wide range of tropical and subtropical mangrove ecosystems of the Atlantic (Bahamas, Bermuda, Brazil, Cuba, East Mexico, Florida in the USA, Sierra Leone in West Africa and South Africa), Indian (East South Africa, Egypt, India, Java, Kenya, Mauritius, Pakistan, South Australia, Seychelles, Sri Lanka, Sumatra), and the Pacific oceans (Australia, Brunei, China, Hawaii, Japan, Malaysia, New Zealand, Philippines, Singapore, Taiwan, Thailand) (Kohlmeyer and Kohlmeyer 1979; Schmit and Shearer 2003). For example, a total of 99 marine fungi were recorded on decaying woody substrata from mangroves of Thailand (Suetrong et al. 2017), and 37 reported on decaying wood of Avicennia marina from the Red Sea coast of Saudi Arabia (Abdel-wahab et al. 2014). Ninety-two marine fungi were reported from seven different mangrove sites of the Bahamas Islands (Jones and Abdel-Wahab 2005). A total of 64 marine fungi were recorded on woody litter of Rhizophora apiculata and 55 on Avicennia officinalis from mangroves of the Godavari and Krishna deltas of the east coast of India (Sarma and Vittal 2001a). Fifty-eight marine fungi were recorded on Avicennia officinalis and Rhizophora mucronata from Udayavara mangroves of the west coast of India (Maria and Sridhar 2003).
Salt marshes are a vital borderline coastal ecosystem determined by tidal movement and are formed by the interface of the halophytic vegetation and sediment from inundating water. Studies on marine fungi associated with diverse salt marsh plants shows no overlap between the fungal decay communities, which highlights the specificity of the chemical and structural characteristics of each plant (Newell and Porter 2002; Blum et al. 2004; Torzilli et al. 2006). Studies on salt marsh plants such as Spartina alterniflora, Juncus roemerianus, and Phragmites australis have indicated a rich diversity of marine fungi similar to many woody mangrove plants (Fell and Hunter 1979; Cuomo et al. 1982, 1985; Poon and Hyde 1998; Barata 2002; Kohlmeyer and Volkmann-Kohlmeyer 2002; Wong and Hyde 2002; Van Ryckegem and Verbeken 2005). The salt marsh plant Suaeda maritima is commonly distributed in India and across several countries, and Suaeda monoica is less commonly found. To our knowledge, the latter salt marsh plant has not been surveyed for marine fungi, while few marine fungi have been documented for the former. Muthupet mangroves include a vast area of salt marsh plants with species such as Suaeda monoica and Suaeda maritima distributed in the intertidal zone.
The objectives of the study were to document fungal diversity of a mangrove habitat previously not surveyed; to determine if host substrates support different fungal communities; and to survey fungi occurring on the salt marsh plant Suaeda monoica at Muthupet mangrove, Tamil Nadu, India.
Materials and methods
Study site and sample collection
Studies on mangrove fungi were carried out from 2015 to 2018. Intertidal and attached dead and decomposing mangrove wood and stem pieces of Aegiceras corniculatum, Avicennia marina, Excoecaria agallocha, Rhizophora mucronata, and Suaeda monoica were collected from Muthupet mangroves (10.4°N, 79.5°E), Kaveri River Delta, Tamil Nadu, southeast coast of India (Fig. 1) Natural earth (2012), QGIS Development team (2016). Samples were placed in sterile plastic bags and transported to the laboratory. The mangrove plants Acanthus ilicifolius and Suaeda maritima were collected from the same geographic area but only during the first 2 years of the survey (2015 and 2016). If needed, mud and debris were washed from samples under running tap water. Samples were incubated in a plastic box lined with a layer of sterile tissue paper and kept moist by spraying with sterile seawater and stored at room temperature until examined (Kohlmeyer and Kohlmeyer 1979). There are mainly two seasons in India: summer (January to June) and rainy (July to December). The fungal colonization and percentage of occurrence of marine fungi on mangrove samples were determined during these seasons.
Morphological studies, isolation, and characterization
The direct examination method was carried out, with magnifications between 7 and 45 × using an Optika stereo zoom SZM-LED1 microscope allowing the images of the ascomata, pycnidia, synnemata, and basidiomata located on the twigs to be captured. The fruiting bodies were cut with a sterile razor blade, and the contents of the ascomata were scooped out for microscopic examination under a compound microscope. Microslides were prepared by mounting the fungal material in sterile seawater or lactophenol, and photomicrographs were taken using a Nikon ECLIPSE TiU upright microscope with DIC objectives fitted with Nikon DS-Fi2 digital camera. Measurements were made with Nikon NIS-Elements-Imaging Software version 4.4 program, and images were processed with Adobe Photoshop CS6 updated version 13.0.1 software (Adobe Systems Inc., USA). The fungi observed were then identified based on the latest keys (Kohlmeyer and Volkmann-Kohlmeyer 1991; Hyde and Sarma 2000; Jones et al. 2009). However, for the identification of few asexual species, we referred to earlier and recent literature (Ellis 1971, 1976; Sutton 1980; Seifert et al. 2011).
All the marine fungal cultures were initiated using the single-spore isolation method as outlined in Devadatha et al. (2017). Colony morphology and their growth rate were observed and measured after 3 weeks to ensure that single-spore isolates obtained were of the same species. Pure cultures were deposited at the National Fungal Culture Collection of India (NFCCI), Pune, India. The herbarium materials were deposited at Ajrekar Mycological Herbarium (AMH), Agharkar Research Institute (ARI), Pune, India. The molecular characterization of novel marine fungi was performed as described in Devadatha et al. (2017). Facesoffungi, Index Fungorum, and MycoBank numbers are provided for the new species discovered from this study (Jayasiri et al. 2015).
Statistical analyses
Percentage colonization and frequency of occurrence of each fungus were calculated as follows:
The univariate community statistics used in this study are: (1) number of species in a sample (richness); (2) number of individuals in a sample (abundance); (3) Simpson diversity index (1-D) (Simpson 1949), where D = sum((ni/n)2) where ni is number of individuals of taxon i; (4) Shannon diversity index: H = sum((ni/n)ln(ni/n)), where n is the total number of individuals; (5) evenness, calculated as the logarithm of Shannon diversity (Shannon 1948), divided by the number of taxa as: eH/S, where H is a measure of Shannon diversity and S is the number of taxa; and (6) Margalef’s richness index: (S-1)/ln(n), where S is the number of taxa, and n is the number of individuals. Jaccard’s similarity coefficient (%) M/(M + N) (where M is the number of matches and N stands for total number of taxa) was determined pair-wise for plant type based on the presence or absence of each species. They were calculated using PAST software version 1.89 (Hammer et al. 2001). Two-way ANOVA (followed by Holm-Sidak’s post-hoc method) was applied to evaluate the influence of season (wet and dry) and plant species on species richness of marine fungi (SigmaPlot, version 11, Systat Inc., San Jose, USA). A 1:74 m and a 1:10 m vector polyline shapefile from the natural Earth (NE) river and lakes’ centerlines base data layers were used to derive the final India and Muthupet mangrove location map using QGIS. Upset plot generated by UpSetR (version 1.3.3) was used for the quantitative analysis of overlapping species between the five mangrove plant wood (Lex et al. 2014), instead of Venn diagram. The bar chart was generated using GraphPad Prism 5.03 software for Windows (www.graphpad.com).
Results
Diversity, occurrence, and distribution of marine fungi in Muthupet
The examined Acanthus ilicifolius and Suaeda maritima samples yielded few marine fungi records (< 5) and were excluded from further analysis.
In total, 6215 samples were collected from the intertidal zone of Muthupet mangroves and examined for the presence of marine fungi, with 2198 samples (36.10%) supporting sporulating fungi. Seventy-eight fungal species in 67 genera were recorded, including 56 Ascomycota (72%), two Basidiomycota (2%), and 20 asexual morphs (26%) (Table 1).
Percentage of occurrence was calculated as mentioned in the Materials and Methods section, and frequency groups were defined as follows: very frequent (> 10%), frequent (> 5–10%), infrequent (> 1–5%), and rare (less than 1%) (Table 2). The only fungus occurring very frequently was Verruculina enalia (21.65%); frequent fungi included Rimora mangrovei (9.15%), Marinosphaera mangrovei (9.2%), Okeanomyces cucullatus (8.7%), and Halocryptosphaeria bathurstensis (6%), while infrequent fungi were Paraconiothyrium cyclothyrioides (4.50%), Hysterium rhizophorae (3.5%), Sclerococcum haliotrephum (3.60%), Lulworthia sp. (4.00%), and Farasanispora avicenniae (3.00%) (Table 2).
Percentage fungal diversity among different hosts of Muthupet
Among the different hosts examined, Avicennia marina was found to support the highest number of marine fungi (49), followed by the salt marsh plant Suaeda monoica (34) (Fig. 2).
Twelve marine fungal species were recorded from Aegiceras corniculatum which included nine Ascomycota (75.5%) and three asexual morphs (25%), (Figs. 2, 3), with Hysterium rhizophorae (44.85%), Rimora mangrovei (21.80%), and Verruculina enalia (17.95%) as the most frequently recorded species. Colonization of A. corniculatum substrates by marine fungi was 38.7% (Table 3). Two new country records (Falciformispora lignalitis, Hysterium rhizophorae) were recorded for A. corniculatum. Photomicrographs of the propagules of the marine fungi recorded in the present study are included in figure plates (Fig. 4a–dd; Fig. 5a–bb; and Fig. 6a–t).
Forty-nine marine fungal species belonging to 44 genera were recorded from Avicennia marina, which included 37 Ascomycota (75.5%), two Basidiomycota (4.0%), and 10 asexual morphs (20.4%) (Figs. 2, 3). Verruculina enalia (27.40%) was found to be the most frequently recorded fungus on this host followed by Marinosphaera mangrovei (12.00%), Halocryptosphaeria bathurstensis (9.25%), Okeanomyces cucullatus (8.70%), Rimora mangrovei (6.15%), Sclerococcum haliotrephum (6.00%), and Paraconithyrium cyclothyroides (4.00%). Colonization of A. marina by marine fungi was 35.4% (Table 3).
Seventeen marine fungal species belonging to 17 genera were recorded from Excoecaria agallocha which included 11 Ascomycota (64.7%) and six asexual fungi (35.2%) (Figs. 2, 3). Verruculina enalia (41.11%) was found to be the most frequent fungus followed by Rimora mangrovei (13.33%), Antennospora quadricornuta (7.77%), Arenariomyces trifurcatus (6.66%), and Halenospora varia (4.44%), with 17.7% of substrates colonized by fungi (Table 3).
Twenty marine fungal species belonging to 19 genera were recorded from Rhizophora mucronata which included 12 Ascomycota (60%), one Basidiomycota (5%), and seven asexual morphs (35%) (Figs. 2, 3). Lulworthia sp. (14.55%) was found to be the most frequent fungus followed by Sammeyersia grandispora (12.2%), Phoma sp. (10.8%), Rimora mangrovei (7.98%), Okeanomyces cucullatus (7.98%), Verruculina enalia (6.57%), Cytospora rhizophorae (6.14%), and Halocyphnia villosa (4.2%). Colonization of R. mucronata by marine fungi was 42.2% (Table 3). Morosphaeria muthupetensis is recorded as specific to this host.
Thirty-four marine fungal species belonging to 32 genera were recorded on Suaeda monoica including 23 Ascomycota (67.5%), two Basidiomycota (5.8%), and nine asexual morphs (26.4%) (Figs. 2, 3). Rimora mangrovei (14.05%) was found to be the most frequent fungus followed by Farasanispora avicenniae and Peroneutypa indica (13.10%), Paraconithyrium cyclothyrioides (11.10%), Okeanomyces cucullatus (8.65%), Verruculina enalia (8.65%), and Marinosphaera mangrovei (7.15%). Colonization of S. monoica by marine fungi was 44.4% (Table 3).
Statistical analyses
Species richness was greatest for Avicennia marina followed by Suaeda monoica and Rhizophora mucronata. Shannon-Weiner index accounting for entropy in an ecosystem was greatest for A. marina, S. monoica, and R. mucronata but lower in Aegiceras corniculatum. A similar profile was observed by the Simpson index indicating that Aegiceras corniculatum has lower diversity in comparison with other plants. Evenness was highest in R. mucronata and lowest in A. marina, hinting that it may have a single species dominance (Table 4 and Table 5).
A two-way ANOVA showed that fungal species richness was significantly affected by plant species (P < 0.001) but not by season (P = 0.239) (Table 6). There was no significant effect of season on fungal richness (season × plant, P = 0.369). Based on multiple comparisons with the Holm-Sidak method, a significant difference was observed in the overall species richness between Avicennia marina and Aegiceras corniculatum, Avicennia marina and Excoecaria agallocha, Avicennia marina and Rhizophora mucronata, Avicennia marina and Suaeda monoica (P < 0.001), and Suaeda monoica and Aegiceras corniculatum (P = 0.003) (Table 6).
Discussion
The current number of accepted marine fungi in the world is 1692 species in 685 genera, 222 families, and 88 orders as listed in the website: marinefungi.org (28 Sep 2020). A significant proportion of that is accounted for by the number documented for mangrove habitats especially over the past 10 years (Suetrong et al. 2017; Sarma 2016).
Current status of marine fungal diversity in Indian mangroves
A total of 850 mangrove fungi have been reported from different mangroves distributed across the world (Devadatha et al. 2021). The number of marine fungi recorded for India is (339) greater than other countries surveyed, e.g., Thailand (303) and Malaysia (171) (Devadatha et al. 2021). Sarma and Devadatha (2020) listed 414 mangrove fungi, including the lower marine fungi, from Indian mangroves. A comparison of fungal diversity between east (225 marine fungi) and west coast (306) of India showed that 117 species were common to both coasts (Sarma and Devadatha 2020). The current study demonstrated that Muthupet mangroves have a rich marine fungal diversity with 20% of total recorded for India. These studies highlight the rich fungal diversity of India reflecting the widespread and extensive areas of mangroves on the east and west coasts.
Marine fungi initially described elsewhere from Muthupet mangroves
Fungal species diversity at Muthupet mangrove was higher (78 taxa) when compared to other tropical locations: Mauritius (67 species, (Poonyth et al. 1999)); Seychelles (63 species, (Hyde and Jones 1989)), Andaman and Nicobar Islands, India (63 species, Chinnaraj (1993)); and Belize (46 species, (Kohlmeyer and Volkmann-Kohlmeyer 1987)), with lower numbers reported for Mandai mangrove, Singapore (41 species, (Tan et al. 1989)).
The survey of Muthupet mangroves resulted in the discovery of many new taxa and have been described elsewhere. These include three novel genera: Thyridariella (T. mangrovei, T. mahakoshae) (Devadatha et al. 2018a), Pseudoastrosphaeriellopsis (P. kaveriana) (Phookamsak et al. 2019), and Raghukumaria (R. keshaphalae) (Jones et al. 2020). The new species described from Muthupet mangroves include: Vaginatispora microarmatispora (Devadatha et al. 2017), Pontoporeia mangrovei (Devadatha and Sarma 2018), Deniquelata vittalii (Devadatha et al. 2018c), Morosphaeria muthupetensis (Devadatha et al. 2018b), Amphisphaeria mangrovei, Hypoxylon teeravasati, Zopfiella indica (Phookamsak et al. 2019), Halocryptosphaeria avicenniae (Dayarathne et al. 2020b), Lanspora cylindrospora, Verruconis mangrovei (Hyde et al. 2020b), Biatriospora borsei (Hongsanan et al. 2020), Fusicolla bharathavarshae (Jones et al. 2020), Peroneutypa polysporae, P. indica, Phaeoseptum carolshearerianum, and Ph. manglicola (Dayarathne et al. 2020a). The fact that of the 78 species recorded 3 are new genera and 20 are new species indicates a rich marine fungal diversity in this mangrove formation. The main reason could be the new host plant Suaeda monoica examined. Our study demonstrates the value of exploring new mangrove locations and host substrates. Hence, further fungal diversity can be expected when mangrove forests hitherto not surveyed, such as mangroves in Africa, Bangladesh, China, Indonesia, Myanmar, Pakistan, South America, and Sri Lanka, are investigated (Hyde and Jones 1989; Jones et al. 2019).
First report of pathogenic marine fungi in Muthupet mangroves
From this study, it is evident that pathogenic fungi, often reported from humans and other sources, may also occur in the marine environment. For example, the sexual and asexual morphs of the human pathogen Medicopsis romeroi were recovered from woody stems of Suaeda monoica. Medicopsis romeroi is commonly reported from mycetoma in humans and immunocompromised hosts and also occasionally on plant materials. Paraconithyrium cyclothyrioides (asexual morph) is a coelomycetous fungal species recognized as an opportunistic pathogen in immunocompromised patients and causes cutaneous phaeohyphomycosis (Gordon et al. 2012). The sexual morph of P. cyclothyrioides was also frequently recorded on S. monoica (Hyde et al. 2020a). Similarly, we have found Scedosporium aurantiacum as a saprobe on decaying woody stems of the halophyte S. monoica from marine habitats. Scedosporium aurantiacum is an opportunistic human pathogen known to cause various infections in lungs, ears, respiratory sinuses, and subcutaneous abscess in patients of diabetes and malignant lymphoma (Kondo et al. 2018).
Core mangrove fungi
Various researchers have attempted to characterize core mangrove fungi, but this is difficult as the study methods and documentation differ (Hyde et al. 1998; Sarma and Hyde 2001; Alias et al. 2010; Sridhar et al. 2012). The most frequent fungi from Muthupet mangroves were Verruculina enalia, Rimora mangrovei, Marinosphaera mangrovei, Okeanomyces cucullatus, and Halocryptosphaeria bathurstensis. According to earlier reports, the most frequent marine fungi from east coast of India were V. enalia, Rimora mangrovei, Halocryptosphaeria bathurstensis, Rhizophila marina, Sclerococcum haliotrephum, Halorosellinia oceanica, and Halocyphnia villosa (Sarma and Vittal 2000; Sarma and Hyde 2001; Sarma et al. 2001). Aniptodera mangrovei, Hydea pygmea, Lignincola laevis, and Savoryella lignicola are the core marine fungi documented for the Indian west coast (Maria and Sridhar 2002, 2003, 2004; Sridhar and Maria 2006). The frequency of occurrence of mangrove fungi differs significantly among different studies; normally, few fungi will dominate a given area, whereas others will be infrequently encountered (Cooke and Rayner 1984, Sarma and Hyde 2001, Sarma et al. 2001).
Prevalence of Ascomycota in mangroves
The Ascomycota is the predominant group of fungi in the marine environment, as in our study, while Basidiomycota is poorly represented (Alias et al. 1995; Sarma and Vittal 2001a; Binder et al. 2006; Vittal and Sarma 2006; Jones et al. 2019). Worldwide a total of 21 filamentous marine basidiomycetes in 17 genera and 75 marine basidiomycete yeasts in 26 genera were recorded in marine environments (marinefungi.org). Of these, 19 filamentous basidiomycetes in 14 genera and 39 basidiomycete yeasts in 20 genera were recorded from mangrove habitats (Devadatha et al. 2021). Only two basidiomycetes were reported in comparison to 56 Ascomycetes in the present study. However, basidiomycetes, like Ganoderma sp., Hexogonia sp., and Schizophyllum commune, were noted on the aerial parts of mangrove trees of Muthupet. In general, the basidiomes of marine Basidiomycota are small and rarely greater than 5 mm. Several reasons have been advanced to explain why so few basidiomata-forming basidiomycetes are reported from the marine environment, and these include wave action which may hamper formation of larger fruiting structures and need to tolerate tidal fluctuations and immersion in seawater and formation and dispersal of basidiospores in an aquatic environment (Jones 1982; Binder et al. 2001; Jones et al. 2019). Ascomycetes are better adapted to an aquatic habitat with minute or microscopic ascomata, often immersed in the host substrate, passive release of ascospores, and or active discharge in the intertidal region.
Host specificity and common mangrove fungi among different hosts were collected during 2015 to 2018
Studies of mangrove fungi suggest they are not host specific, with the exception of those growing on the brackish water palm Nypa fruticans with Loilong et al. (2012) listing 31 that are unique to this host, e.g., Anthostomella nypae, Bacusphaeria nypae, Fasciatispora nypae, Helicascus nypae, Manglicola guatemaelensis, Pleurophomopsis nypae and Tirisporella baccariana (Jones et al. 1996; Hyde and Alias 1999; Suetrong et al. 2009; Loilong et al. 2012; Abdel-Wahab et al. 2017). To date, most mangrove fungi have been found growing on woody substrates, while plants in the salt marsh zones of mangroves have been little studied in the tropics, e.g., Suaeda monoica. In the current study, we examined the colonization of five timber host plants, and the results are presented in UpSet plot (Fig. 7). Fewer fungi were recorded on two mangrove associates: Acanthus ilicifolius and Suaeda maritima as collections were made only in 2015–2016 with fewer samples, and hence, they were not accounted in ecological observations. The herbaceous nature of these substrata seems to be not favorable for fungal colonization, in contrast to other mangrove plants. UpSet plot indicates that A. marina supported 19 unique fungal species, while S. monoica and R. mucronata have 11 each, while E. agallocha and R. mucronata have four unique fungal taxa (Fig. 7). Only four fungal taxa (Lulworthia sp., Okeanomyces cucullatus, Rimora mangrovei, Verruculina enalia) were found to be common to all host substrates, indicating that certain fungal species have very particular niche colonization. Few host-specific marine fungi have been found in this study. However, six species are specific to Avicennia marina (Biatrispora borsei, Halocryptosphaeria avicenniae Fusicolla bharatavarshae, Hypoxylon teeravasti, Thyridariella mangrovei, and T. mahakoshae), five to Suaeda monoica (Amphisphaeria mangrovei, Deniquelata vittalii, Lanspora cylindrospora, Peroneutypa indica, and P. polysporae), two to A. corniculatum (Raghukumaria keshaphale and Vaginatispora microarmatispora), and one to Rhizophora mucronata (Morosphaeria muthupetensis). These taxa are recently introduced, and further studies are required to determine if they are host specific. It is interesting to note that Suaeda maritima, which is more common in mangroves throughout the world, did not support a rich fungal diversity. This may be attributed to the herbaceous nature of S. maritima, while S. monoica is woody. This study is the first to document the colonization of woody tissues of S. monoica and again demonstrates the need to sample a wider range of host mangrove plants. Many low- and high-salt marsh plants also form part of the mangrove ecosystem such as Juncus kraussii in Australia and remain to be surveyed for fungi (Sainty et al. 2012).
Species richness, diversity, and evenness of marine fungi recovered from Muthupet mangroves
A higher species richness and fungal incidence was observed in Aviccenia marina followed by S. monoica compared to other plant species (Fig. 2). The higher occurrence of marine fungi on A. marina and S. monoica may be due to larger number of available substrata and greater susceptibility to colonization. Another reason is dominance of A. marina and S. monoica plants when compared to other mangrove plants in Muthupet. However, two exceptions are E. agallocha and S. maritima. Even though these plants are dominant in Muthupet, they did not support a rich fungal diversity. The evenness was lower in A. marina, while it was highest in R. mucronata possibly due to dominant fungal species in A. marina (H. bathurstensis, V. enalia and M. mangrovei) indicating that R. mucronata harbors an even fungal community on it. Simpson’s diversity index (1-D) was highest for R. mucronata followed by S. monoica and A. marina indicating that R. mucronata harbored a highly diverse fungal species compared to the other tree species. Margalef’s index and Shannon index are dependent on the total number of species and were hence higher in A. marina and S. monoica (Table 4).
Conclusions
Despite several studies on mangrove fungi, many mangrove sites in India remain unexplored. This also applies to many other countries with extensive mangroves: Africa, Australia, and South America. Previous studies of Indian mangroves yielded circa 17 new marine fungi. In the current study, 78 marine fungal taxa were reported, of which three were new genera and 19 new species, which were reported elsewhere (Devadatha et al. 2017, 2018a, b, c, 2019, Devadatha and Sarma 2018, Dayarathne et al. 2020a, b, Hongsanan et al. 2020, Hyde et al. 2020b, Jones et al. 2020, Phookamsak et al. 2019). This highlights the need for intensive sampling supported by sequencing data. Reports of marine fungi from mangrove soil and leaf litter are few in number; hence, further studies are required to explore their diversity in mangroves. Additional studies are required to reveal the fungal community structure associated with decomposition of mangrove plants, including metagenomic/transcriptomic-based analyses on marine fungi from mangrove litter, soil, water, and wood in order for a better understanding of the nature of fungal interactions in mangroves. While these surveys enhance our knowledge of the diversity of marine fungi in mangrove ecosystems, studies involving high-throughput sequencing techniques are urgently required to form a more robust statistical evaluation of fungal activity and occurrence of non-sporulating taxa.
References
Abdel-wahab MA, Hodhod MS, Bahkali AHA, Jones EBG (2014) Marine fungi of Saudi Arabia. Bot Mar 57:323–335. https://doi.org/10.1515/bot-2014-0010
Abdel-Wahab MA, Dayarathne MC et al (2017) New saprobic marine fungi and a new combination. Bot Mar 60:469–488. https://doi.org/10.1007/s13225-019-00426-5
Alias SA, Kuthubutheen AJ, Jones EBG (1995) Frequency of occurrence of fungi on wood in Malaysian mangroves. Hydrobiologia 295:97–106
Alias SA, Zainuddin N, Jones EBG (2010) Biodiversity of marine fungi in Malaysian mangroves. Bot Mar 53:545–554. https://doi.org/10.1515/BOT.2010.066
Barata M (2002) Fungi on the halophyte Spartina maritima in salt marshes. Fungi Mar Environ 179–193
Binder M, Hibbett DS, Molitoris HP (2001) Phylogenetic relationships of the marine gasteromycete Nia vibrissa. Mycologia 93:679–688. https://doi.org/10.1080/00275514.2001.12063199
Binder M, Hibbett DS, Wang Z, Farnham WF (2006) Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte. Am J Bot 93:547–556. https://doi.org/10.3732/ajb.93.4.547
Blum LK, Roberts MS, Garland JL, Mills AL (2004) Distribution of microbial communities associated with the dominant high marsh plants and sediments of the United States east coast. Microb Ecol 48:375–388
Borse BD, and Hyde KD (1989) Marine fungi from India. III. Acrocordiopsis patilii gen. et. sp. nov. from mangrove wood. Mycotaxon
Borse BD, Borse KN, Pawar NS, Tuwar AR (2013) Marine fungi from India-XII. A revised check list. IJMS 42:110–119
Borse BD, Pawar NS, Patil SY et al (2018) Aquatic fungi of India: fresh water and marine. BIOINFOLET-A Q J Life Sci 15:137–148
Chinnaraj S (1993) Higher marine fungi from mangroves of Andaman and Nicobar Islands. Sydowia 45:109–115
Chinnaraj S, Untawale AG (1992) Manglicolous fungi from India. Indian J Geo-Marine Sci 25:25–29
Cooke RC, Rayner ADM (1984) Ecology of saprophytic fungi. London: Longman
Cuomo V, Vanzanella F, Fresi E et al (1982) Micoflora delle fenerogame dellIsola d’Ischia: Posidonia oceanica (L.) Delile Cymodocea nodosa (Ucria) Aschers. Bull Mus Inst Biol Univ Genova 50:162–166
Cuomo V, Vanzanella F, Fresi E et al (1985) Fungal flora of Posidonia oceanica and its ecological significance. Trans Br Mycol Soc 84:35–40
Dayarathne MC, Jones EBG, Maharachchikumbura SSN et al (2020a) Morpho-molecular characterization of microfungi associated with marine based habitats. Mycosphere 11:1–188. https://doi.org/10.5943/mycosphere/11/1/1
Dayarathne MC, Wanasinghe DN, Devadatha B et al (2020b) Modern taxonomic approaches to identifying diatrypaceous fungi from marine habitats, with a novel genus Halocryptovalsa Dayarathne & KD Hyde, gen. nov. Cryptogam Mycol 41:21–67. https://doi.org/10.5252/cryptogamie-mycologie2020v41a3
Devadatha B, Sarma V (2018) Pontoporeia mangrovei sp. nov, a new marine fungus from an Indian mangrove along with a new geographical and host record of Falciformispora lignatilis. Curr Res Environ Appl Mycol 8:238–246. https://doi.org/10.5943/cream/8/2/8
Devadatha B, Sarma VV, Wanasinghe DN et al (2017) Introducing the new Indian mangrove species, Vaginatispora microarmatispora (Lophiostomataceae) based on morphology and multigene phylogenetic analysis. Phytotaxa 329:139–149. https://doi.org/10.11646/phytotaxa.329.2.4
Devadatha B, Sarma VV, Jeewon R et al (2018a) Thyridariella, a novel marine fungal genus from India: morphological characterization and phylogeny inferred from multigene DNA sequence analyses. Mycol Prog 17:1–14. https://doi.org/10.1007/s11557-018-1387-4
Devadatha B, Sarma VV, Jeewon R, Jones EBG (2018b) Morosphaeria muthupetensis sp. nov.(Morosphaeriaceae) from India: morphological characterization and multigene phylogenetic inference. Bot Mar 61:395–405. https://doi.org/10.1515/bot-2017-0124
Devadatha B, Sarma VV, Ariyawansa HA, Jones EBG (2018c) Deniquelata vittalii sp. nov., a novel Indian saprobic marine fungus on Suaeda monoica and two new records of marine fungi from Muthupet mangroves East Coast of India. Mycosphere 9:565–582. https://doi.org/10.5943/mycosphere/9/3/8
Devadatha B, Mehta N, Baghela A, Sarma VV (2019) Vittaliana mangrovei gen. et sp. nov. in Phaeosphaeriaceae from Pondicherry mangroves in India, based on morphology and multigene phylogeny. Cryptogamie Mycologie 40:117–132. https://doi.org/10.5252/cryptogamiemycologie2019v40a7
Devadatha B, Jones EBG, Pang KL, Abdel-Wahab MA, Hyde KD, Sakayaroj J, Bahkali AH, Calabon M, Sarma VV, Sutreong S Zhang S (2021) Occurrence and geographical distribution of mangrove fungi. Fungal Divers 106:137–227. https://doi.org/10.1007/s13225-020-00468-0
Ellis MB (1971) Dematiaceous hyphomycetes. Kew: Commonwealth Mycological Institute
Ellis MB (1976) More dematiaceous hyphomycetes. Kew: Commonwealth Mycological Institute, 507
Fell JW, Hunter IL (1979) Fungi associated with the decomposition of the black rush, Juncus roemerianus, in south Florida. Mycologia 322–342
Gordon RA, Sutton DA, Thompson EH et al (2012) Cutaneous phaeohyphomycosis caused by Paraconiothyrium cyclothyrioides. J Clin Microbiol 50(11):3795–3798. https://doi.org/10.1128/JCM.01943-12
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Hongsanan S, Hyde KD, Phookamsak R et al (2020) Refined families of dothideomycetes: Dothideomycetidae and pleosporomycetidae. Mycosphere 11:1553–2107. https://doi.org/10.5943/mycosphere/11/1/13
Hyde KD, Jones EBG (1988) Marine mangrove fungi. Mar Ecol 9:15–33
Hyde KD, Jones EBG (1989) Ecological observations on marine fungi from the Seychelles. Bot J Linn Soc 100:237–254
Hyde KD, Lee SY (1995) Ecology of mangrove fungi and their role in nutrient cycling: what gaps occur in our knowledge? Hydrobiologia 295:107–118
Hyde KD, Alias SA (1999) Linocarpon angustatum sp. nov., and Neolinocarpon nypicola sp. nov. from petioles of Nypa fruticans, and a list of fungi from aerial parts of this host. Mycoscience 40:145–149. https://doi.org/10.1007/BF02464293
Hyde KD, Sarma VV (2000) Pictorial key to higher marine fungi. Mar Mycol a Pract approach Fungal Divers Press Hong Kong 86
Hyde KD, Jones EBG, Leaño E et al (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161
Hyde KD, Norphanphoun C, Abreu VP et al (2017) Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Divers 87:1–235. https://doi.org/10.1007/s13225-017-0391-3
Hyde KD, Chaiwan N, Norphanphoun C, Boonmee S et al (2018) Mycosphere notes 169–224. Mycosphere 9:271–430. https://doi.org/10.5943/mycosphere/9/2/8
Hyde KD, de Silva NI, Jeewon R et al (2020a) AJOM new records and collections of fungi: 1–100. Asian J Mycol 3:22–294. https://doi.org/10.5943/ajom/3/1/3
Hyde KD, Dong Y, Phookamsak R et al (2020b) Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers 100:5–277. https://doi.org/10.1007/s13225-020-00439-5
Jayasiri SC, Hyde KD, Ariyawansa HA et al (2015) The faces of fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Divers 74:3–18
Jones EBG (1982) Decomposition by basidiomycetes in aquatic environments. In: Symposium series-British Mycological Society
Jones EBG (2011) Are there more marine fungi to be described? Bot Mar 54:343–354. https://doi.org/10.1515/bot.2011.043
Jones EBG, Abdel-Wahab MA (2005) Marine fungi from the Bahamas Islands. Bot Mar 48:356–364. https://doi.org/10.1515/BOT.2005.048
Jones EBG, Read SJ, Moss ST et al (1996) Tirisporella gen. nov., an ascomycete from the mangrove palm Nypa fruticans. Can J Bot 74:1487–1495. https://doi.org/10.1139/b96-179
Jones EBG, Sakayaroj J, Suetrong S et al (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:187
Jones EBG, Pang K-L, Abdel-Wahab MA et al (2019) An online resource for marine fungi. Fungal Divers 96:347–433. https://doi.org/10.1007/s13225-019-00426-5
Jones EBG, Devadatha B, Abdel-Wahab MA et al (2020) Phylogeny of new marine Dothideomycetes and Sordariomycetes from mangroves and deep-sea sediments. Bot Mar 63:155–181. https://doi.org/10.1515/bot-2019-0014
Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Southward, AJ, Tyler, PA, Young, CM Fuiman, LA (eds), New York: Adv Mar Biol Acad Press, 40:84–251. https://doi.org/10.1016/S0065-2881(01)40003-4
Kathiresan K, Rajendran N (2005) Mangrove ecosystems of the Indian Ocean region. IJMS 34:104–113
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. New York: Acad Press. https://doi.org/10.1016/C2013-0-10998-1
Kohlmeyer J, Volkmann-Kohlmeyer B (1987) Marine fungi from Belize with a description of two new genera of ascomycetes. Bot Mar 30:195–204. https://doi.org/10.1515/botm.1987.30.3.195
Kohlmeyer J, Volkmann-Kohlmeyer B (1991) Illustrated key to the filamentous higher marine fungi. Bot Mar 34:1–61. https://doi.org/10.1515/botm.1991.34.1.1
Kohlmeyer J, Volkmann-Kohlmeyer B (2002) Fungi on Juncus and Spartina: new marine species of Anthostomella, with a list of marine fungi known on Spartina. Mycol Res 106:365–374. https://doi.org/10.1017/S0953756201005469
Kondo M, Goto H, Yamanaka K (2018) Case of Scedosporium aurantiacum infection detected in a subcutaneous abscess. Med Mycol Case Rep 20:26–27. https://doi.org/10.1016/j.mmcr.2018.01.003
Lex A, Gehlenborg N, Strobelt H et al (2014) UpSet: visualization of intersecting sets. IEEE Trans vis Comput Graph 20:1983–1992
Loilong A, Sakayaroj J, Rungjindamai N, et al (2012) 15 Biodiversity of fungi on the palm Nypa fruticans. Mar Fungi Fungal-like Org 273. https://doi.org/10.1515/9783110264067
Maria GL, Sridhar KR (2002) Richness and diversity of filamentous fungi on woody litter of mangroves along the west coast of India. Curr Sci 1573–1580
Maria GL, Sridhar KR (2003) Diversity of filamentous fungi on woody litter of five mangrove plant species from the southwest coast of India. Fungal Divers 14:109–126
Maria GL, Sridhar KR (2004) Fungal colonization of immersed wood in mangroves of the southwest coast of India. Can J Bot 82:1409–1418. https://doi.org/10.1139/b04-090
Naskar K, Mandal R (1999) Ecology and biodiversity of Indian mangroves. Daya Books
Natural Earth, Natural Earth Geo Features. Natural earth large scale 1:10 m data of river+lakes centerlines V 2.0, 2012. [Online]. http://www.naturalearthdata.com/downloads/10m-physical-vectors/10m-rivers-lake-centerlines/
Newell SY, Porter D (2002) Microbial secondary production from salt marsh-grass shoots, and its known and potential fates. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Springer, pp 159–185. https://doi.org/10.1007/0-306-47534-0_9
Patil SD, Borse BD (1983) Marine fungi from Maharashtra (India) III. Some fungi from mangroves. Indian Bot Reports 2:56–58
Patil SD, Borse BD (1985) Marine fungi from Indian mangroves. The mangroves proceedings on the national symposium on the biological utilization and conservation of Mangroves. Shivaji University Publication, Kolhapur, pp 151–152
Phookamsak R, Hyde KD, Jeewon R, et al (2019) Fungal diversity notes 929–1035: taxonomic and phylogenetic contributions on genera and species of fungi. Fungal Divers 1–273. https://doi.org/10.1007/s13225-019-00421-w
Pointing SB (1999) Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Divers 2:17–33
Poon MOK, Hyde KD (1998) Biodiversity of intertidal estuarine fungi on Phragmites at Mai Po marshes, Hong Kong. Bot Mar 41:141–156. https://doi.org/10.1515/botm.1998.41.1-6.141
Poonyth AD, Hyde KD, Peerally A (1999) Intertidal fungi in Mauritian mangroves. Offpr Bot Mar 42:243–252. https://doi.org/10.1515/BOT.1999.028
QGIS Development Team (2016) QGIS geographic information system (version 3.12.1). Software. https://www.qgis.org
Raveendran K, Manimohan P (2007) Marine fungi of Kerala: a preliminary floristic and ecological study. Malabar Natural History Society. https://doi.org/10.13140/2.1.3699.8084
Ravikumar DR, Vittal BPR (1996) Fungal diversity on decomposing biomass of mangrove plant Rhizophora in Pichavaram estuary, east coast of India. IJMS 25:142–144
Sainty GR, Hosking J, Carr G, Adam P (2012) Estuary plants and what’s happening to them in south-east Australia. Sainty Books
Sarma VV (2016) Diversity of mangrove fungi on Rhizophora wood in Puducherry, Southeast coast of India. KAVAKA 46:37–39
Sarma VV, Hyde KD (2001) A review on frequently occurring fungi in mangroves. Fungal Divers 8:1–34
Sarma VV, Raghukumar S (2013) Manglicolous fungi from Chorao mangroves, Goa, West coast of India: diversity and frequency of occurrence. Nov Hedwigia 97:533–542
Sarma VV, Vittal BPR (2000) Biodiversity of mangrove fungi on different substrata of Rhizophora apiculata and Avicennia spp. from Godavari and Krishna deltas, east coast of India. Fungal Divers 5:23–41
Sarma VV, Vittal BPR (2001a) Biodiversity of manglicolous fungi on selected plants in the Godavari and Krishna deltas, east coast of India. Fungal Divers 6:115–130
Sarma VV, Devadatha B (2020) Fungal diversity in mangroves of India and a note on their medicinal potential. In: Patra JK, Mishra RR, Thatoi H (eds) Biotechnological utilization of mangrove resources. Elsevier, pp 153–224. https://doi.org/10.1016/B978-0-12-819532-1.00007-X
Sarma VV, Hyde KD, Vittal BPR (2001) Frequency of occurrence of mangrove fungi from the east coast of India. Hydrobiologia 455:41–53. https://doi.org/10.1023/A:1011983200976
Schmit JP, Shearer CA (2003) A checklist of mangrove-associated fungi, their geographical distribution and known host plants. Mycotaxon 85:423–477
Seifert K, Jones MG, Gams W, Kendrick B (2011) The genera of hyphomycetes. CBS Biodiversity series no. 9:1–997. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423
Shearer CA, Descals E, Kohlmeyer B et al (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16:49–67. https://doi.org/10.1007/s10531-006-9120-z
Simpson EH (1949) Measurement of diversity. Nature 163:688
Singh AK, Ansari A, Kumar D, Sarkar UK (2012) Status, biodiversity and distribution of mangroves in India: an overview. Uttar Pradhesh Sate Biodivers Board Mar Biodivers One Ocean Many Worlds Life 59–67
Sridhar KR (2009) Fungal diversity of Pichavaram mangroves, southeast coast of India. Nat Sci 7:1545–1740
Sridhar KR, Maria GL (2006) Fungal diversity on mangrove woody litter Rhizophora mucronata (Rhizophoraceae). Indian J Geo-Marine Sci 35:318–325
Sridhar KR, Alias SA, Pang K-L (2012) Mangrove fungi. In: Jones EBG, Pang KL. Marine fungi and fungal-like organisms. de Gruyter, Berlin, Germany, 2012. pp 253–271. https://doi.org/10.1515/9783110264067
Suetrong S, Schoch CL, Spatafora JW et al (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173. https://doi.org/10.3114/sim.2009.64.09
Suetrong S, Preedanon S, Klaysuban A et al (2017) Distribution and occurrence of manglicolous marine fungi from eastern and southern Thailand. Bot Mar 60:503–514. https://doi.org/10.1515/bot-2016-0107
Sutton BC (1980) The Coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Kew: Commonwealth Mycological Institute, 1–696 pp
Tan TK, Leong WF, Jones EBG (1989) Succession of fungi on wood of Avicennia alba and A. lanata in Singapore. Can J Bot 67:2686–2691. https://doi.org/10.1139/b89-346
Torzilli AP, Sikaroodi M, Chalkley D, Gillevet PM (2006) A comparison of fungal communities from four salt marsh plants using automated ribosomal intergenic spacer analysis (ARISA). Mycologia 98:690–698. https://doi.org/10.1080/15572536.2006.11832641
Van Ryckegem G, Verbeken A (2005) Fungal diversity and community structure on Phragmites australis (Poaceae) along a salinity gradient in the Scheldt estuary (Belgium). Nov Hedwigia 80:173–197
Vittal BPR, Sarma VV (2006) Diversity and ecology of fungi on mangroves of Bay of Bengal region - an overview. Indian J Mar Sci 35(4):308–317
Wong MKM, Hyde KD (2002) Fungal saprobes on standing grasses and sedges in a subtropic aquatic habitat. Fungal Divers Res Ser 7:195–212
Acknowledgements
V.V. Sarma would like to thank the Ministry of Earth Sciences (MOES), Govt. of India (MOES/36/OOIS/Extra/40/2014/PC-IV) for funding this work. He also would like to thank the Tamil Nadu Forest Department and District Forest Office, Tiruvarur, Tamil Nadu, for providing permission to collect samples. Department of Biotechnology, Pondicherry University, is thanked for providing the facilities. B. Devadatha would like to thank the Ministry of Earth Sciences, Govt. of India, for providing a fellowship. VVS thanks UGC-SAP and DST-FIST programs of Govt. of India for partial infrastructural support. E. B. Gareth Jones was supported under the Distinguished Scientist Fellowship Program (DSFP), King Saud University, Kingdom of Saudi Arabia. We thank the anonymous reviewers for their comments and suggestions which have improved the manuscript.
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This research was funded by the Ministry of Earth Sciences (MOES), Govt. of India, grant number (MOES/36/OO1S/Extra/40/2014/PC-IV).
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BD contributed in the investigation of the research work, methodology, formal analysis, software, data curation, writing the original draft of the manuscript, review, editing, and visualization. SG contributed in the statistical analyses, software, formal analysis, writing-review, editing type face, and data curation. EBG has contributed in review and editing of the manuscript, visualization and validation. VVS contributed in conceptualization, methodology, resources, supervision, project administration, funding acquisition, and review and editing of the manuscript. All authors reviewed and approved the manuscript.
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Bandarupalli, D., Jones, E.B.G., Ghate, S.D. et al. Biodiversity of marine fungi in mangroves with reference to Muthupet mangroves, Tamil Nadu, east coast of India. Mar. Biodivers. 51, 88 (2021). https://doi.org/10.1007/s12526-021-01214-8
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DOI: https://doi.org/10.1007/s12526-021-01214-8