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Monographs used to identify the morphology of fungi are Isolation of fungi from mangroves
Standard Manuals of Marine Mycology, the Higher
Fungi, Compendium of Soil Fungi and Genera of Hypho- According to Behera et al.2, mangrove forests are bio-
mycetes2,25,27. diversity hotspots for marine fungi. Mangroves signify
The micro-features of pure culture can be identified by intermediate vegetation sandwiched by land and sea,
semi-permanent microscopic preparations of fungi using which is growing in waterlogged soil with lack of oxy-
lactophenol cotton blue stain. A drop of lactophenol cot- gen. The mangroves soil substrata are generally firm to
ton blue stain is placed on a clean slide before transfer- soft mud with aerial roots known as pneumatophores
ring a small tuft of fungus with a sterilized inoculating which emerge from substratum to supply air36. Soil is
loop. Then the slides are gently heated to release air bub- among the essential habitats for microorganisms such as
bles, if any, on the glass cover and later observed under bacteria, fungi, nematodes, etc. and also a general reser-
the microscope with oil immersion objective6,17,25,28,29. voir for wind-dispersed fungal spore4.
Identification of fungi can also be done genetically Gupta13 reported fungal diversity of different mangrove
and is often used to confirm the initial morphological areas with varying salinity. There were 45 fungi isolated
identification. The most common marker used for species representing 5 genera (Scutellospora C. Walker & F. E.
identification and phylogenetic analysis is the ITS (inter- Sanders, Glomus Tul. & C. Tul., Gigaspora Gerd. &
nal transcribed spacer) region. Trappe, Entrophospora R.N. Ames & R.W. Schneid. and
Acaulospora Gerd. & Trappe). Majority of fungi that
Isolation of fungi from forest ecosystems were found in low salinity areas belonged to the genus
Glomus, and the presence of two Glomus species
Different species of soil fungi are found in forest areas [Glomus intraradices N.C. Schenck & G.S. Sm. and G.
across the world. The most common fungi in forest soils geosporum (T.H. Nicolson & Gerd.) C. Walker] in high-
are Aspergillus Micheli, Penicillium Link, Trichoderma salinity areas suggests the possibility of habitat adapta-
Pers. and Fusarium Link. They have been found in vari- tion to salt tolerance13. Li et al.37 studied the endophytic
ous types of forest soils such as yellow–brown forest soil, communities in four different mangroves species in China
raw calcareous soil, yellow soil, red soil, mountain– and found that overall colonization frequency on the four
meadow soil and brown forest soil30, as well as from dark host trees varied from 24% to 33%. Colonization was
brown forest soil, brown coniferous forest soil, mountain also seen to be higher in twigs compared to leaves. Three
grass forest soil and mountain tundra soil31. hundred and one fungal isolates were obtained from vari-
Several studies have discussed the isolation and cha- ous samples and ITS sequencing indicated that Phomop-
racterization of various strains of fungi from different sis Sacc. & Roum., Phyllosticta Pers., Xylaria Hill ex
forests around the world. Isolation of Trichoderma, Fusa- Schrank, Leptosphaerulina McAlpine and Pestalotiopsis
rium, Acremonium Link, Penicillium and Paecilomyces Steyaert were dominant in all host species.
Samson from Brazilian Savannah and Atlantic rainforest The fungal colonization in grey mangroves, Avicennia
has been reported32. In Nanga Merit Forest, Sarawak, marina (Forssk.) Vierh. of Red Sea, Saudi Arabia has
Malaysia, isolates of Penicillium and Streptomyces been studied. Six samples were collected and 145 species
Waksman & Henrici have been characterized33. Paecilo- were identified. Ascomycota was dominant (76–85%) in
myces marquandii (Massee) S. Hughes, Aspergillus fla- all samples followed by Basidiomycota (14–24%). The
vus Link, A. fumigatus Fresenius, Mucor hiemalis prevalence of Ascomycota in mangroves areas is
Wehmer, Penicillium sp., Cladosporium herbarum (Pers.) expected as their lignocelluloses cleaving capabilities are
Link, Trichosporiella cerebriformis (G.A. de Vries & important in areas that are rich in lignin and cellulose,
Kleine-Natrop) W. Gams, Mortierella sp. Coem., Synce- and these fungi would allow the substrates to enter the
phalastrum recemosum Cohn and Cunninghamella echi- food web. Aspergillus and Schizosaccharomyces Lindner
nulata (Thaxt.) Thaxt. ex Blakeslee were identified from were found to dominate the soil areas1.
Bhadra Wildlife Sanctuary in the Western Ghats, India,
comprised of dry and moist deciduous, semi-evergreen
and evergreen forests34. Another study carried out in the Isolation of fungi from coastal areas
same area by Banakar and Thippeswamy35 revealed other
fungal species, such as Chaetomium globosum Kunze, Fungi are known to exist in marine environments since
Thelephora terrestris Ehrh., Humicola sp. Traaen, Tala- the early times38. The ocean reflects a great reservoir of
romyces sp. C.R. Benj., Trametes versicolor (L.) Lloyd, biodiversity. The marine environment is exceptionally
Trametes hirsuta (Wulfen) Lloyd, Phanerochaete sordida complex and comprises a broad variety of fungal diver-
(P. Karst.) J. Erikss. & Ryvarden, Lenzites betulina (L.) sity39,40. Marine fungi are a taxonomically diverse group,
Fr., Pleurotus ostreatus (Jacq.) P. Kumm., Stereum ost- developing in many different habitats within the marine
rea (Blume & T. Nees) Fr. and Phanerochaete chrysos- ecosystems, including sea water, corals, algae, marine
porium Burds. sediments, etc.41,42. These marine fungi can be sub-divided
into two groups: (1) obligate or residents, and (2) faculta- plant–fungus relationships are ectomycorrhizal (ECM)
tive or transient fungi. Obligate marine fungi grow and and arbuscular mycorrhizal (AM). ECM is characterized
sporulate exclusively in marine or estuarine environments by the formation of a fungal coating on the root surfaces
whereas facultative marine fungi inhabit terrestrial or and of hyphal network penetrating between the cortical
freshwater habitats, but are capable of growing and spo- cells and endodermis, known as Hartig net50. This type is
rulating in marine environments41. Marine-derived fungi usually associated with coniferous and deciduous trees.
have been found in several places such as sediment, However, AM is typically associated with herbaceous
sponges, algae, fish, deep sea and mangrove wood43. The plants and grasses, and is characterized by the formation
interest in marine ecology has also increased worldwide. of arbuscules within the root cortical cells51,52.
Several substrata in marine environments are good These mycorrhizal symbioses enhance plant growth by
sources for the detection of fungi38. Marine fungi have allowing the soil to be more efficiently utilized, resulting
numerous ecological roles such as degradation of biota, in more uptake of nutrients such as nitrogen and phospho-
provision of chemical protection, pathogenicity, symbi- rus, as well as increasing the plant defence mechanism
osis and impact on various holobiont groups42. Some ma- against natural stresses. Nitrogen plays an important part
rine fungi are key decomposers of organic matter, and in plant morphology, photosynthesis, formation of nucle-
others are involved in the denitrification process41 and ic acids and enzymes, whereas phosphorus is needed for
hence are considered as a source of industrial enzymes44. cell division, reproduction and metabolism51. In return,
Beena et al.45 carried out a study on the diversity of the fungi benefit from these photosynthesizing plants as
fungi from the coastal sand dunes in India, and isolated the fungi have direct access to the carbohydrates translo-
38 species from 5 genera (Scutellospora, Glomus, Gigas- cated from the leaves into the roots.
pora, Sclerocystis Berk. & Broome and Acaulospora) The mycoheterotrophic relationship of three common
with Glomus mosseae (T.H. Nicolson & Gerd.) Gerd. & shrubs of the family Pyroleae found on the northern side
Trappe being the most dominant. Séne et al.15 studied the of Mt Fuji, Japan, with ECM fungi was studied. Pyrola
diversity of ectomycorrhizal fungi in Coccoloba uvifera alpina H. Andres, P. incarnata (DC.) Freyn and Orthilia
(L.) L. mature trees, and found 8 species colonizing the secunda L. were found to have shared similar mycobionts
sporocarps and sclerotia whereas 15 species were found with the surrounding trees, Larix kaempferi (Lamb.)
on the root tips, with the seedlings sharing 14 of these Carr., Abies veitchii Lindley and Betula ermanii Cham,
taxa. Scleroderma bermudense Coker, Russula cremeoli- but at different levels. P. incarnata shared almost 70%
lacina Pegler and Thelephoraceae were dominant. S. mycobionts with the surrounding trees, whereas P. alpina
bermudense had the potential to form a common and O. secunda shared 32% and 15% respectively. O. se-
mycorrhizal network between the mature trees and cunda was exclusively associated with Wilcoxina sp.
seedlings, for increasing the survival chances of the Chin S. Yang & Korf, an ECM fungus, suggesting an
seedlings. independent mycorrhizal association. A more diverse
Parveen et al.46 explored the fungal diversity in Maha- community of ECM fungi was found in the other two
nadi River, India. There were 31 fungal species isolated, Pyrola species, with a higher percentage of shared myco-
with Aspergillus niger Tiegh. being the most prominent. bionts53.
Another study in 2016 had isolated 8 fungal genera (As- Some orchid plants from the forests in Thailand, par-
pergillus, Penicillium, Thielavia Zopf, Fusarium, Emeri- ticularly Aphyllorchis montana Rchb. f, A. caudate Rolfe
cella Berk., Cladosporium Link, Scytalidium Pesante and ex Downie and Cephalanthera exigua Seidenf. were
Alternaria Nees) from Masturah, Saudi Arabia47. Most found to have mycoheterotrophic association with ECM
isolated fungi showed significant growth on petroleum fungi. A. montana and A. caudata showed a diverse ECM
media and hence have the potential for biodegrading community, majority of which were Russulaceae and
crude oil-based substances. Since 1957, the Japanese An- Thelephoraceae. The latter was also found predominantly
tarctic Research Expedition has isolated 76 fungal species in C. exigua (65%), but the same orchid species did not
from the Syowa Station, East Antarctica. Majority of show high ECM diversity as in the other two species,
these fungi were Ascomycota and Basidiomycota. They which could be due to its short roots54.
were able to survive in harsh conditions such as low tem- de Souza and Freitas55 compared AM fungi of an exotic
peratures and lack of nutrients48. invasive plant, Prosopis juliflora (Sw.) DC. and a native
plant, Mimosa tenuiflora (Willd.) Poir. that grow in the
tropical seasonal dry forest in Brazil. In both plants, sig-
Isolation of mycorrhizal fungi nificant differences were observed in fungal composition
as well as in the soil chemical factors such as soil pH,
Fungi that form localized hyphae interfaces have syn- total organic carbon, total nitrogen and availability of
chronized development with the host plants and benefit phosphorus. A total of 29 species of AM fungi were
the host plants via nutrient transfer are known as mycorr- found in all of the soil samples with the orders Glome-
hizae49. The most common types of these symbiotic rales (44.8%) and Gigasporales (41.4%) and the genus
CURRENT SCIENCE, VOL. 116, NO. 5, 10 MARCH 2019 735
REVIEW ARTICLE
Funneliformis C. Walker & A. Schüßler being the most stress had reduced the growth of Pinus muricata D. Don.
prevalent. The soils where P. juliflora developed had A total of 82 species were isolated, and preferential root
higher chemical factors, but only consisted of AM fungi colonizers such as Suillus tomentosus (Kauffman) Singer
from the orders Diversisporales, Gigasporales and Glo- and Russula brunneola Burl. were found on pygmy and
merales. The soils where M. tenuiflora developed also nonpygmy host plants respectively. It was also found that
had AM fungi from the same orders but also with the the trees from the more stressful environment were pre-
order Archaeosporales, making the AM community more ferentially colonized by ECM fungi with more carbon-
diverse. intense foraging strategies62.
Swietenia macrophylla King seedlings and mature trees
growing in a tropical rainforest in Mexico, were studied
for their AM fungal communities. Almost 23 fungi were Isolation of endophytic fungi
isolated and classified into 4 genera. The diversity of AM
fungi in the mature trees composed of Glomus (52.3%), Endophytic fungi live within plant tissues, such as leaves,
Acaulospora (38%), Ambispora C. Walker, Vestberg & twigs, branches and roots63. These fungi produce metabo-
A. Schüssler and Gigaspora (4.7% each). Acaulospora lites that generally cause no harm to the plants, but can
(63.6%) and Glomus (36.3%) were isolated from the increase the survival fitness of the hosts63,64. Differences
seedlings56. Lang et al.57 studied the diversity of mycorr- in the species composition of fungal endophytes can be
hizal species in mixed deciduous forests in Germany. A observed in trees with different growth rates, as shown in
total of 130 ECM fungal species were detected on the a study where 43 fungi were identified from 360 twigs of
root tips of host plants (Fagus sp. L., Tilia sp. L. and Pinus sylvestris L. (Scots pine) in northern Spain65. The
Carpinus sp. L.). These species colonized 92.8% of the most abundant fungi were from the classes Dothideomy-
root tips, and AM fungi were abundant in the roots of cetes and Sordariomycetes. The endophytic community
Fraxinus sp. L. and Acer sp. L. between fast- and slow-growing pines was found to be
Souza and Rodrigues studied the diversity of AM fungi different, with Phoma herbarum Westend. occupying the
in three mangrove species (Acanthus ilicifolius L., Ex- twigs of fast-growing trees while Hypocrea lixii Pat. was
coecaria agallocha L. and Rhizophora mucronata Lam.) associated with the slow-growing trees65.
from two mangrove forests in India and during different Rojas-Jimenez et al.66 explored the diversity of endo-
seasons (pre-monsoon, monsoon and post-monsoon). phytic fungi along an altitudinal gradient (400–2900 m)
A total of 11 AM fungi from five genera (Rhizophagus in tropical forests of Costa Rica. They found that the
P.A. Dang., Glomus, Funneliformis, Racocetra Oehl, lower the altitude, the higher was the species richness of
F.A. Souza & Sieverd. and Acaulospora) were isolated endophytic fungi; also particular preference to plant host
from all sites and during all seasons. Species richness and for fungi in higher altitudes was uncommon. Almost 92%
spore density were recorded highest in pre-monsoon sea- of these isolates were from the class Sordariomycetes.
son and lowest in monsoon season. The high spore densi- Colletotrichum Corda, Diaporthe Nitschke and Xylaria
ty in pre-monsoon season could be explained by soil were dominant at different altitudes since many years.
temperature, as higher temperature favours AM fungal The diversity of fungal endophytes in Fortunearia
sporulation, or by other factors58. Studies of ECM fungi sinensis Rehder & E.H. Wilson growing in mixed ever-
from mangroves are limited as the fungal communities in green/deciduous broadleaved forest in Jiangsu Province,
mangroves are typically AM59. China was studied67. Almost 1436 strains were isolated
In a study, coastal sands and reclamation sites in Icel- from the laminae, petioles and twigs of F. sinensis that
and were examined for AM fungal abundance60. On the were collected during spring and autumn. These isolates
coastal sand plain, AM fungi were not found on the bar- were classified into 33 genera with Alternaria (21.52%),
ren sand, while some were discovered in a natural old Fusarium (19.64%) and Pestalotiopsis (13.16%) being
dune system and in the reclamation sites of Leymus are- the dominant ones. The genus Alternaria was commonly
narius (L.) Hochst. However, the older reclamation site found in both seasons. However, Pestalotiopsis and
had a higher number of AM fungi compared to new sites. Chaetomium Kunze were more abundant in spring, while
The same was observed on the volcanic island of Surtsey. Fusarium and Monotospora Corda in autumn. The diver-
Different AM inocula of L. arenarius revealed that indi- sity of endophytic fungi in F. sinensis was higher in the
genous AM fungi were able to improve the growth of petioles than laminae and twigs67.
seedlings60. A study was carried out on a New Zealand In the Western Ghats, Pestalotiopsis spp. were isolated
dune, where root samples of Spinifex sericeus R.Br. were from 58 tree species from 4 types of forests (dry thorn,
collected61. A total of 22 AM fungal operational taxonomic dry deciduous, stunted montane evergreen and moist
units (OTUs) were identified and classified into 7 genera; deciduous). The frequency varied from 0.7% to 41.0% with
the dominant genera were Rhizophagus and Racocetra. regard to forest type and tree host. ITS sequencing deter-
The association of ECM fungi and trees in relation to mined that 28 of these isolates, which were identified (on
environmental stress was examined, where environmental the basis of morphology) as Pestalotiopsis, were discovered
736 CURRENT SCIENCE, VOL. 116, NO. 5, 10 MARCH 2019
REVIEW ARTICLE
as 2 genera, i.e. Pestalotiopsis and Neopestalotiopsis degradation of pollutants are increased by adding mate-
Maharachch., K.D. Hyde & Crous. Pestalotiopsis isolates rials such as fertilizers or microbes into the affected
were identified as P. microspora (Speg.) G.C. Zhao & N. areas. Because fungi use hydrocarbons as their food
Li, P. vismiae (Petr.) J. Xiang Zhang & T. Xu, P. mene- source, they can be used to degrade oil in the case of an
zesiana (Bres. & Torrend) Bissett, P. parva Maharachch., oil spill71.
K.D. Hyde & Crousand P. theae (Sawada) Steyaert, while Quite a number of fungi have been isolated from con-
Neopestalotiopsis isolates were identified as N. cubana taminated coastal and marine areas. Several fungi were
Maharachch., K.D. Hyde & Crous and N. mesopotamica isolated from beaches in the Gulf of Mexico (Fusarium,
Maharachch., K.D. Hyde & Crous, N. australis Maha- Scopulariopsis Bainier and Aspergillus)72, coastal areas
rachch., K.D. Hyde & Crous, N. ellipsospora (Maha- of the Red Sea in Saudi Arabia [Alternaria alternata (Fr.)
rachch. & K.D. Hyde) Maharachch., K.D. Hyde & Crous, Keissl., Aspergillus flavus, A. fumigatus, A. niger, A. och-
N. piceana Maharachch., K.D. Hyde & Crous and N. sa- raceus K. Wilh., A. sydowii (Bainier & Sartory) Thom &
prophytica (Maharachch. & K.D. Hyde) Maharachch., Church, A. terreus Thom, Penicillium chrysogenum Thom,
K.D. Hyde & Crous. It was concluded that Pestalotiopsis P. oxalicum Currie & Thom, P. rugulosum Thom, Scopu-
spp. are not host-specific endophytes and can be found in lariopsis brumptii Salv.-Duval and Ulocladium atrum
many different tree species68. Preuss]47, and a Mediterranean marine site (A. terreus,
Gazis and Chaverii19 examined the leaves and stems of Trichoderma harzianum and P. citreonigrum Dierckx)73.
wild rubber trees (Hevea brasiliensis Müll. Arg.) that Several fungi (Aspergillus niger, A. ochraceus and
were found in the Amazon basin, Peru. A total of 175 iso- Penicillium chrysogenum) were able to degrade six n-
lates were obtained, resulting in the identification of 58 alkanes (tridecane, tetradecane, pentadecane, hexadecane,
OTUs. Ascomycota represented 96.6% of these isolates. heptadecane, octadecane) and crude oil74. Fungi can also
Sapwood samples were found to have a higher diversity degrade other types of oil, such as gasoline. Rhizopus
of endophytes than leaf samples, with Pestalotiopsis aff. arrhizus A. Fisch. was isolated from a gasoline-polluted
Palmarum (Cooke) Steyaert and Trichoderma harzianum mangrove swamp in Nigeria11. Rhodotorula aurantiaca
Rifai dominating leaf and sapwood samples respectively. (Saito) Lodder and Candida ernobii (Lodder & Kreger)
The wild rubber trees contained a higher diversity of S.A. Mey. & Yarrow, isolated from Suape Port in Brazil,
beneficial fungal species and less potentially pathogenic were able to degrade diesel oil compounds75. While other
species than plantation trees. In particular, they found species were able to degrade used engine oil, e.g. Asper-
that there were 2.5 times more Trichoderma strains in the gillus flavus, A. niger, Rhodotorula rubra (Schimon) F.C.
wild trees than plantation trees19. Harrison and Torulopsis candida Lodder76.
It was observed in a study that endophytic fungi from Saravanan and Sivakumar77 highlighted the potential of
healthy leaves of Theobroma cacao L., which were iso- marine ecosystem fungi as hydrocarbon bio-degraders by
lated from several localities, including tropical forest in isolating them from coastal deltaic habitat along the east
the Republic of Panama, had restricted the in vitro growth coast (Bay of Bengal) of India. A total of 41 species were
of the three most common cacao pathogens, namely enumerated from five different sampling stations with
Moniliophthora roreri (Cif.) H.C. Evans, Stalpers, Sam- Aspergillus being the most common genus represented by
son & Benny (frosty pod rot), Phytophthora palmivora 14 species. This was followed by Cladosporium with five
(E.J. Butler) E.J. Butler (black pod rot), and Monilioph- species, Penicillium with six species and Fusarium with
thora perniciosa (Stahel) Aime & Phillips-Mora (witches three species. Ten fungal species were chosen for qualita-
broom)69. It was also found that one Trichoderma isolate tive determination of their ability in biodegrading hydro-
had parasitized M. roreri. The study shows the potential carbons. Trichoderma viride Pers. had grown well in
of using endophytic fungi as biocontrol agents. diesel-added media (24 mm in colony diameter), whereas
Penicillium citrinum Thom in petrol-added media
(90 mm colony diameter).
Biodegradation capability of fungi Mohsenzadeh et al.78 evaluated fungal strains obtained
from an oil refinery in Iran, for their potential in the bio-
Fossil fuels are compounds made up of carbon and remediation of petroleum-polluted soils. It was shown
hydrogen, or hydrocarbons. The variance between differ- that all four fungi were resistant to petroleum pollution.
ent fossil fuels lies in their hydrogen-to-carbon ratio. Alternaria sp. showed the highest resistance to 10%
Crude oils are mainly used to generate electricity, whereas petroleum pollution with 47.50 mm colony diameter
petroleum and natural gas are used to manufacture che- compared to the other three fungal strains, Aspergillus
micals, plastics, paints and many other products, while terreus (31.25 mm), Penicilium sp. (23 mm) and Acre-
gasoline and diesel fuels are used in transportation. How- monium sp. (20.50 mm)78. Adekunle and Adeniyi79 iso-
ever, fossil fuels are non-renewable and raise severe envi- lated fungi from Treculia africana Decne. seeds in
ronmental concerns70. Biodegradation of oil can be done Nigeria and assessed their hydrocarbon biodegradation
by bioremediation, in which the rates of natural bio- capabilities. Six fungi were examined for the study and
CURRENT SCIENCE, VOL. 116, NO. 5, 10 MARCH 2019 737
REVIEW ARTICLE
measurements were carried out every five days by assess- metabolic capacity are promising candidates for mycore-
ing the turbidity of the media. Rhizopus sp. Ehrenb. was mediation. Fungal applications range from the uptake of
found to be the best in degrading oil for all oil types used toxic heavy metals to degradation of textile dyes, pesti-
in the study while the least was found to be Penicillium cides and polycyclic aromatic hydrocarbons. Hence
pinophilum Hedgcock. mycoremediation offers a cost-effective and environ-
Aranda et al.80 studied the biodegradation mechanism ment-friendly alternative to decontamination of the
of isolated fungi from a polluted pond in Granada, Spain. polluted environment. Understanding metabolic pathways
Among the tested samples, ten fungi were identified and and advanced genomic research will help shed light on
screened for degradation capabilities against anthracene, the intricate processes of fungal survival, adaptability and
phenanthrene, dibenzothiophene and dibenzofuran, which remediation strategies. Their non-specific enzyme sys-
are common polyaromatic hydrocarbons (PAHs). PAHs tems, robust protein machinery, diverse morphology and
are typically present in areas that have been polluted with absorption capacities offer excellent tools for biodegrada-
fuel or oil. Penicillium oxalicum completely degraded tion of contaminants. It would also be interesting to
anthracene whereas the others were only able to partially develop products of mycoremediation for large-scale
degrade it (8–81%). The time-course study found that P. application. This article may further contribute to the
oxalicum was able to completely degrade anthracene and substantial potential offered by fungal diversity in various
dibenzothiophene within four days. The other two PAHs habitats and their bioremediation potential.
were also degraded by the fungi, but at slower rates.
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