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Abstract

Lichens have long been considered as composite organisms composed of algae and/or cyanobacteria hosted by a fungus in a mutualistic relationship. Other organisms have been gradually discovered within the lichen thalli, such as multiple algal species, yeasts, or even viruses. Of pivotal relevance is the existence of the lichen microbiome, which is a community of microorganisms that can be found living together on the lichen surface. This community performs a growing number of functions. In this entry, we explore the journey of lichens being considered from a dual partnership to a multi-species symbiotic relationship.
Citation: Morillas, L.; Roales, J.; Cruz,
C.; Munzi, S. Lichen as Multipartner
Symbiotic Relationships. Encyclopedia
2022,2, 1421–1431. https://doi.org/
10.3390/encyclopedia2030096
Academic Editors: Milva Pepi and
Raffaele Barretta
Received: 5 May 2022
Accepted: 25 July 2022
Published: 3 August 2022
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4.0/).
Entry
Lichen as Multipartner Symbiotic Relationships
Lourdes Morillas 1, 2, * , Javier Roales 1,3 , Cristina Cruz 1and Silvana Munzi 1,4
1Center for Ecology, Evolution and Environmental Changes & CHANGE—Global Change and
Sustainability Institute, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Bloco C2,
1749-016 Lisbon, Portugal; jroabat@upo.es (J.R.); ccruz@fc.ul.pt (C.C.); ssmunzi@fc.ul.pt (S.M.)
2Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Av. Reina Mercedes 10,
41080 Seville, Spain
3
Departamento de Sistemas Físicos, Químicos y Naturales, Universidad Pablo de Olavide, Ctra. Utrera Km 1,
41013 Seville, Spain
4Centro Interuniversitário de História das Ciências e da Tecnologia, Faculdade de Ciências,
Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal
*Correspondence: lmorillas@fc.ul.pt
Definition:
Lichens have long been considered as composite organisms composed of algae and/or
cyanobacteria hosted by a fungus in a mutualistic relationship. Other organisms have been gradually
discovered within the lichen thalli, such as multiple algal species, yeasts, or even viruses. Of pivotal
relevance is the existence of the lichen microbiome, which is a community of microorganisms that
can be found living together on the lichen surface. This community performs a growing number of
functions. In this entry, we explore the journey of lichens being considered from a dual partnership
to a multi-species symbiotic relationship.
Keywords: symbiosis; microbiome; partnership; mycobiont; photobiont; holobiont; bacterial layer
1. General Context of Lichens
Lichens are just one of many symbiotic relationships that can be established between
heterotrophic fungi and photoautotrophic partners, such as plants, mosses, cyanobacte-
ria, and algae. Partnerships between fungi and vascular plants are highly diverse and
ecologically relevant. Some of these partnerships, such as those of ectomycorrhizas [
1
],
endomycorrhizas, or the unique orchid mycorrhizal associations [2], are well known. The
relationships between fungi and cyanobacteria or algae are also well known and very
diverse, including the relation between algicolous fungi and bacteria or algae [
3
] and
lichens [
4
]. Algicolous fungi can parasitize algae or cyanobacteria [
5
,
6
] or alternatively can
establish a mutualistic relationship, as in the case of mycophycobioses [
7
]. Lichen-forming
fungi may establish symbiotic relationships with algae or cyanobacteria and form a unique
identity, i.e., the lichen. However, although unique, lichens are just one example of the
highly diverse partnerships between fungi and photosynthetic organisms.
More than 18,000 fungal species, comprising a highly diverse group and representing
around 20% of those currently identified, participate in lichen partnerships. They occur
in all terrestrial ecosystems, ranging from polar to tropical areas and from coastal to high
mountain ecosystems. Lichens form vegetative structures called thalli and can grow on
a large variety of substrates such as minerals, rocks, bare soil, and the wood or leaves of
plants, even in streams and marine zones [8], as well as on synthetic material surfaces.
The symbiotic condition of lichens remained unknown for a long time and, until
1869 [
9
], they were thought to be individual organisms. The German mycologist Anton de
Bary introduced the term “symbiosis” to describe the condition of dissimilar organisms
living together [
10
] supporting Schwendener’s theory that lichen is formed by two separate
organisms, a fungus and an alga. From then on, lichens were considered to be an obligate
partnership between a fungus (mycobiont) and either cyanobacteria and/or green algae,
Encyclopedia 2022,2, 1421–1431. https://doi.org/10.3390/encyclopedia2030096 https://www.mdpi.com/journal/encyclopedia
Encyclopedia 2022,21422
that acted as a photoautotrophic partner (photobiont) [
8
,
11
]. Figure 1shows the location of
the mycobiont and the photobiont within heteromerous lichens, in which the algae and
fungal components are arranged in definite layers. The stability of this symbiotic associa-
tion depends on the mutualistic–antagonistic relationships of a multitude of interlinked
organisms, also known as the “holobiont” [
12
,
13
]. This complex relationship is determined
by the symbionts’ interactive intimacy, stability of environmental conditions, and partner
availability [14,15].
Encyclopedia 2022, 1, FOR PEER REVIEW 2
that acted as a photoautotrophic partner (photobiont) [8,11]. Figure 1 shows the location
of the mycobiont and the photobiont within heteromerous lichens, in which the algae and
fungal components are arranged in definite layers. The stability of this symbiotic
association depends on the mutualistic–antagonistic relationships of a multitude of
interlinked organisms, also known as the “holobiont [12,13]. This complex relationship
is determined by the symbionts’ interactive intimacy, stability of environmental
conditions, and partner availability [14,15].
Figure 1. (a) Correspondence between the lichen structure and (b) their individual components in a
heteromerous thallus. Depiction of tripartite lichen (c) and homoiomerous lichen (d).
Thalli are specialized structures unique to lichen-forming fungi and are not observed
when the mycobiont grows in isolation. The thalli hold the photosynthetic partners and
are one of the most complex structures in the entire fungal kingdom. Thallus structures
are mainly determined by the fungal partner and can be grouped into three main growth
forms: crustose, foliose, or fruticose. Crustose lichens, lacking the lower cortex, are
completely attached to the substrate, while foliose and fruticose lichens are only partially
attached through anchor like structures such as rhizines and hapters [16]. The internal
space of the thallus can be made up of either an internal stratification with a fungal upper
layer and underlying algal layer (heteromerous, Figure 1a), or an even distribution of the
Figure 1.
(
a
) Correspondence between the lichen structure and (
b
) their individual components in a
heteromerous thallus. Depiction of tripartite lichen (c) and homoiomerous lichen (d).
Thalli are specialized structures unique to lichen-forming fungi and are not observed
when the mycobiont grows in isolation. The thalli hold the photosynthetic partners and are
one of the most complex structures in the entire fungal kingdom. Thallus structures are
mainly determined by the fungal partner and can be grouped into three main growth forms:
crustose, foliose, or fruticose. Crustose lichens, lacking the lower cortex, are completely
attached to the substrate, while foliose and fruticose lichens are only partially attached
through anchor like structures such as rhizines and hapters [16]. The internal space of the
thallus can be made up of either an internal stratification with a fungal upper layer and
underlying algal layer (heteromerous, Figure 1a), or an even distribution of the mycobiont
and photobiont (homoiomerous, Figure 1d). Lichens do not have a waxy cuticle to isolate
Encyclopedia 2022,21423
the thalli from their surroundings and therefore everything in the lichen’s environment is
absorbed into its structure, including water and nutrients coming from air and rain. They
also lack vascular tissues (such as xylem and phloem in plants) to distribute nutrients and
water around their thalli.
The general structure of a heteromerous lichen is shown in Figure 1and it is mainly
composed of layers of fungus and alga. The upper cortex is the outer layer of the lichen
thallus, and it is formed by the mycobiont. The cells in this layer are tightly packed to
provide certain physical and chemical protection from the environment. The algal layer
contains the photobiont, which frequently is a green alga. Cyanobacteria, if present, can be
located in small vacuoles called cephalopodiums, which exist on top of the upper cortex or
within the tissues of the lichen when there is a green algal layer already present (secondary
photobiont, Figure 1c), or in a layer under the upper cortex (primary photobiont). Part
of the lichen thallus is composed of filamentous fungal cells that form the medulla. This
layer is loosely packed and has a threadlike structure. The lower cortex, with a similar
structure to the upper cortex, protects the medulla and give support to the rhizines or
other basal attachments that allow lichens to get linked to their substrate. Rhizines are
fungal multicellular structures originated on the lower surface with no vascular purposes:
no water or nutrients can be absorbed by them, and their unique function is to support
the lichen attachment. Although this is the most frequent structural organization found
in a thallus, some lichens present no distinguishable layers of mycobiont and photobiont.
In these cases, the components are distributed in one big uniform layer, resulting in a
gelatinous growth form (Figure 1d).
Most lichen-forming fungi belong to the phylum Ascomycota, while only 0.3% of
lichenized fungi are known to be derived from Basidiomycota [
8
,
17
]. The majority of
lichen-forming algae belong to the green algae (85%), and 10% have a cyanobacterium as
primary photosynthetic partner, but also brown or yellow-green algae have been identified
in these relationships [
18
,
19
]. Sexual reproduction of the fungal partner involves the growth
of fruiting bodies from the thallus which produce ascospores to be dispersed. In addition to
this sexual mechanism, lichens have also developed other processes of asexual reproduction
to disperse both partners together in varied and specific joint propagules [16].
2. From a Dual Partnership to a Multi-Species Symbiotic Relationship
In this intimate and long-term partnership, the fungal partner provides water, mineral
nutrients, and sheltering structures for the photobiont, which contributes photosyntheti-
cally fixed carbon as the energy source for the system. Although the fungus can be very
specific when selecting its photobiont [
20
,
21
], generalist fungi have also been frequently
described [
22
25
]. Yahr et al. [
26
] established three categories according to the range of
photobionts with which they are able to lichenize: photobiont specialists, intermediates and
generalists. Following this scheme, photobiont specialists partner with single algal lineages,
while photobiont generalists accept a high variety of algal partners and can stablish associ-
ations with a number of strains according to environmental conditions. Intermediates form
symbiotic relationships with a reduced number of algal partners. Photobiont generalists are
frequently associated to lichens with wide both geographical range and ecological niches,
which can associate with locally adapted photobionts in different climatic regions [
25
,
27
,
28
].
The exact factors that determine the photobiont selection are well known and appear to
be related to phylogenetic specialization, fungus reproductive strategy, photobiont cell
availability and ecological factors such as climate or substrate [
29
,
30
]. Surprisingly, multiple
algal species have been observed in association with the same thallus in a large number
of studies [
24
,
31
,
32
]. For example, Backor et al. [
33
] confirmed the presence of multiple
algal genopypes in a single lichen thallus, Casano et al. [
34
] found that Ramalina farinacea
thalli represent a specific and selective form of symbiotic association involving the same
two Trebouxia phycobionts, and Del Campo et al. [
35
] concluded that ecological diversifi-
cation and speciation of lichen symbionts in different habitats could include a transient
phase consisting of associations with more than one photobiont in individual thalli. This
Encyclopedia 2022,21424
pattern of algal coexistence is probably promoted by their different and complementary
ecophysiological responses which facilitate the proliferation of the lichen in a wide range
of habitats and geographic areas [34].
In the last decade, it has been shown that lichens are far from being a simple asso-
ciation between two unrelated organismal groups, and instead involve a bacterial (and
other fungi including yeast) component which is a key contributor to the biology of the
holobiont. The inclusion of bacteria within the lichen partnership was first observed around
the 1930’s
[3638]
(Figure 2), and it has been described as a discontinuous monolayer on the
thallus surface (Figure 1). At that time, rudimentary methods only facilitated associating
these bacteria with a possible and unspecific role in nitrogen fixation. At the beginning of
the 21st century, the first molecular analyses started using bacterial isolates (e.g., Gonza-
lez et al. [
39
]). However, as culture-dependent methods can only account for 0.001–15%
of the bacterial diversity [
40
], most microorganisms had remained unrevealed [
41
]. More
recent studies allowed the observation that the structure of the nitrogen-fixing bacteria
present in the cyanolichens is different from that of chlorolichens and that chlorolichens
have a higher diversity of nitrogen-fixing bacteria than cyanolichens [
42
]. Also, in addition
to the main cyanobiont, other cyanobacteria have been found within the microbiota of
lichen thalli and substrates [
43
,
44
], which can also contribute with part of the nitrogen
input to the symbiosis.
Once new methods were developed to complement the previously applied techniques,
the limitations of the bacterial isolation were overcome, which allowed researchers to
holistically explore the bacterial community. Fingerprinting techniques [
45
] and molecular
cloning methods (e.g., Hodkinson and Lutzoni, [
46
]) allowed the production of microbial
community profiles of lichen-associated microbiota. Bates et al. [
47
] revealed the microbial
community associated with lichens based on next generation pyrosequencing for the first
time. Thus, multi-omics approaches, that allow the integration of multiple omics research
and datasets explaining the mechanisms underlying biological processes and molecular
functions [
48
], along with bioinformatic tools have put the spotlight on the host-specific
bacterial microbiome [
49
52
]. Recent findings about bacterial associations with lichens
support their relationship as a multi-species symbiosis in which different roles are played
by an increasingly recognized diversity of organisms associated with the thalli (see [
49
]
and references therein; Figure 2).
3. Potential Roles of Recently Discovered Partners
Bacterial and secondary fungal communities inhabiting lichens have been found
through next-generation sequencing techniques (e.g., Grube et al. [
45
], Tuovinen et al. [
53
]).
Key roles as functional components in structuring the thalli and modulating the response
to environmental factors could be performed by these overlooked organisms [
49
,
50
,
54
].
Since the first half of the 20th century, individual strains of bacteria have been isolated
from lichens, with Alpha proteobacteria making up the dominant group, first observed by
Cardinale et al. [
55
]. Studies of the diversity of lichen-associated bacteria suggest that dif-
ferent parts of the thallus, providing different chemical and physiological micro-niches, can
influence microbial colonization ([
45
,
46
] and references therein). Another main factor driv-
ing the bacterial composition is the fungal partner. Accordingly, Aschenbrenner et al. [56]
demonstrated that the lichen Lobaria pulmonaria presented a core and shared fraction of its
bacterial biome, as well as a transient fraction. They also demonstrated that bacteria were
present in the lichen’s vegetative propagules which allowed them to vertically transmit
through asexual reproduction. Traditionally, it has been accepted that the mycobiont builds
up the thallus as a result of the specific interaction with a suitable algal partner, and then
numerous associated and potentially interacting bacterial and other partners colonize the
lichen more or less specifically. Recently, it has been hypothesized that the microbiome
contributes to the lichenization process [57].
Similar questions to those posed regarding the role and specificity of bacteria within
lichens have also been raised in relation to secondary fungal communities inhabiting lichens.
Encyclopedia 2022,21425
Spribille et al. [
58
] found that a specific group of basidiomycetous yeasts played a part in
the microbiome of two epiphytic lichens (Figure 2), and that the abundance of the yeast
within the lichen was correlated with concentrations of vulpinic acid, which is a secondary
metabolite associated with lichen defenses. More recently, Cernajova and Skaloud [
59
]
discovered previously unknown cystobasidiomycete symbionts in a number of Cladonia
species in the northern hemisphere.
The consistent presence of basidiomycetous yeast within lichens in these studies sug-
gested these were the third partner within the lichen complex. However, Millanes et al. [
60
]
considered Cyphobasidium spp. to be a lichen-related fungi that can form galls on the
thalli instead of as a previously unseen third mutualistic partner. The relevance of these
lichen-related yeasts was also discussed by Oberwinkler [
61
], who pointed out that “it is
obvious that basidiomycetous yeasts in lichen thalli are not a third component of symbiosis,
but rather the vegetative propagules of mycoparasites”. Supporting this view, Lende-
mer et al. [
51
] failed to detect basidiomycete yeasts in over 97% out of 339 lichen species
from the Appalachian Mountains in North America in a metagenomic study. Although
their metagenomic approach is likely less sensitive than PCR assays with specific primers,
these findings raise questions about the ubiquity and specificity of yeasts in lichens.
Encyclopedia 2022, 1, FOR PEER REVIEW 5
interacting bacterial and other partners colonize the lichen more or less specifically.
Recently, it has been hypothesized that the microbiome contributes to the lichenization
process [57].
Similar questions to those posed regarding the role and specificity of bacteria within
lichens have also been raised in relation to secondary fungal communities inhabiting
lichens. Spribille et al. [58] found that a specific group of basidiomycetous yeasts played
a part in the microbiome of two epiphytic lichens (Figure 2), and that the abundance of
the yeast within the lichen was correlated with concentrations of vulpinic acid, which is a
secondary metabolite associated with lichen defenses. More recently, Cernajova and
Skaloud [59] discovered previously unknown cystobasidiomycete symbionts in a number
of Cladonia species in the northern hemisphere.
The consistent presence of basidiomycetous yeast within lichens in these studies
suggested these were the third partner within the lichen complex. However, Millanes et
al. [60] considered Cyphobasidium spp. to be a lichen-related fungi that can form galls on
the thalli instead of as a previously unseen third mutualistic partner. The relevance of
these lichen-related yeasts was also discussed by Oberwinkler [61], who pointed out that
“it is obvious that basidiomycetous yeasts in lichen thalli are not a third component of
symbiosis, but rather the vegetative propagules of mycoparasites.Supporting this view,
Lendemer et al. [51] failed to detect basidiomycete yeasts in over 97% out of 339 lichen
species from the Appalachian Mountains in North America in a metagenomic study.
Although their metagenomic approach is likely less sensitive than PCR assays with
specific primers, these findings raise questions about the ubiquity and specificity of yeasts
in lichens.
Figure 2. Temporal line indicating the timing at which the different components of the lichen
partnership were discovered. This figure reflects the journey from considering lichens as a single
organism to the complex multipartner symbiotic relationship known nowadays
[9,10,34,36,58,62,63].
Figure 2.
Temporal line indicating the timing at which the different components of the lichen
partnership were discovered. This figure reflects the journey from considering lichens as a single
organism to the complex multipartner symbiotic relationship known nowadays [
9
,
10
,
34
,
36
,
58
,
62
,
63
].
4. The Increasing Complexity Surrounding the Concept of Lichen
The discovery of potential new partners increased the complexity of species interac-
tions within these supraorganisms. However, the lack of experimental evidence regarding
the lichen microbiome hindered our ability to reveal the network of interactions within this
holobiont. As opposed to what was traditionally believed, the photobiont should not be
Encyclopedia 2022,21426
limited to a single strain of algae [
34
] and protists and even viruses can form symbiotic
associations with lichens [62,63] (Figure 2).
Conceptualizing a lichen means accounting for a vast array of related microorganisms,
providing the ideal example of a holobiont, composed of a dominant mycobiont and diverse
microbiome [
64
]. This evolved network of biotic connections whose morphology is shaped
by the mycobiont, is at the service of the fitness of the entire superorganism. Hawksworth
and Grube [
65
] re-defined the lichen symbiosis as: ‘a self-sustaining ecosystem formed
by the interaction of an exhabitant fungus, an extracellular arrangement of one or more
photosynthetic partners and an indeterminate number of other microscopic organisms’ [
66
].
While a detailed analysis of the scientific scrutiny focused on lichens is beyond the
purpose of this text, a rough indication of the increasing interest in the lichen microbiome
can be obtained by looking at the publications of the last 20 years (Figure 3). Although
a linear relationship is missing, since 2014, the concept of a lichen symbiotic association,
including more than just the mycobiont and the photobiont was well established. The
development of “omic” technologies is a key element that has allowed the proliferation of
studies in this research field [
67
]. The number of citations of a specific paper can increase
with the time from its publication, which can explain the low number of citations for the
most recent works; however, since 2015, the annual number of citations has exceeded 50,
testifying to an increasing interest in this specialized topic.
Encyclopedia 2022, 1, FOR PEER REVIEW 6
4. The Increasing Complexity Surrounding the Concept of Lichen
The discovery of potential new partners increased the complexity of species
interactions within these supraorganisms. However, the lack of experimental evidence
regarding the lichen microbiome hindered our ability to reveal the network of interactions
within this holobiont. As opposed to what was traditionally believed, the photobiont
should not be limited to a single strain of algae [34] and protists and even viruses can form
symbiotic associations with lichens [62,63] (Figure 2).
Conceptualizing a lichen means accounting for a vast array of related
microorganisms, providing the ideal example of a holobiont, composed of a dominant
mycobiont and diverse microbiome [64]. This evolved network of biotic connections
whose morphology is shaped by the mycobiont, is at the service of the fitness of the entire
superorganism. Hawksworth and Grube [65] re-defined the lichen symbiosis as: a self-
sustaining ecosystem formed by the interaction of an exhabitant fungus, an extracellular
arrangement of one or more photosynthetic partners and an indeterminate number of
other microscopic organisms’ [66].
While a detailed analysis of the scientific scrutiny focused on lichens is beyond the
purpose of this text, a rough indication of the increasing interest in the lichen microbiome
can be obtained by looking at the publications of the last 20 years (Figure 3). Although a
linear relationship is missing, since 2014, the concept of a lichen symbiotic association,
including more than just the mycobiont and the photobiont was well established. The
development of “omic technologies is a key element that has allowed the proliferation of
studies in this research field [67]. The number of citations of a specific paper can increase
with the time from its publication, which can explain the low number of citations for the
most recent works; however, since 2015, the annual number of citations has exceeded 50,
testifying to an increasing interest in this specialized topic.
Figure 3. Number of papers related to the lichen microbiome and their citations. Data obtained using
the search terms “lichen microbiome” or “lichen microbiota” or “lichen bacterial community or
“lichen microbial” or “lichen bacteria” or “lichen-associated bacteria” in the Web of Science
(https://www.webofscience.com/wos/woscc/basic-search). Accessed on 13 February 2022. All
results were checked to ensure that they were referred to the presence of microorganisms in the
lichen symbiosis.
5. Mutualism or Parasitism?
Although lichens are usually considered mutualistic symbioses, many lichen
characteristics identify them as controlled parasitic interactions [68,69]. Initial studies in
Figure 3.
Number of papers related to the lichen microbiome and their citations. Data obtained
using the search terms “lichen microbiome” or “lichen microbiota” or “lichen bacterial community”
or “lichen microbial” or “lichen bacteria” or “lichen-associated bacteria” in the Web of Science
(https://www.webofscience.com/wos/woscc/basic-search) accessed on 13 February 2022. All
results were checked to ensure that they were referred to the presence of microorganisms in the
lichen symbiosis.
5. Mutualism or Parasitism?
Although lichens are usually considered mutualistic symbioses, many lichen char-
acteristics identify them as controlled parasitic interactions [
68
,
69
]. Initial studies in this
field deemed lichens as algae parasitized by fungi because they found algal cells in a
lichen thallus which were dead or penetrated by fungal haustoria. However, other au-
thors considered lichens as mutualists based on the seemingly healthy and long-lasting
Encyclopedia 2022,21427
relationship among its partners. Two different experimental approaches have been de-
veloped to study selectivity among the lichen partners. The first one is based on
in vitro
resynthesis of the independently cultured mycobiont with different photobiont species.
An alternative approach involves the assessment of the specimens collected in different
geographical areas and the identification of the partners present in the lichen thalli [
70
].
In vitro
studies give researchers the opportunity to observe initial stages of the lichenization
process. Several developmental stages of lichenization have been described depending on
the interacting alga, and timing of these events is variable depending on the species, media,
and incubation conditions. The first developmental stage which has been described is the
“pre-contact” stage, crucial for the establishment of symbiont recognition mechanisms and
biont specificity [
71
,
72
], where the partners are in close proximity to share extracellular
secretions but not physical contact. In a second phase, the “contact” stage, the two bionts
start making physical contact by fungal appressoria (which are flattened hyphal tips that
bind to the host cell surface and start a penetration peg), whereas, in a third phase termed
the “growth together” stage, the two partners grow together in a network to form cellular
masses containing both bionts [7376].
Attempts of resynthesis in the laboratory starting from the isolated partners have
been made with various and inconsistent outcomes [
52
,
68
,
69
,
77
86
], making the study of
lichenization mechanisms hard due to the lack of consistently repeatable results.
In vitro
re-synthesis experiments showed that the interaction of a mycobiont with its compatible
algal partner triggers specific morphological differentiation that is not seen when in contact
with incompatible algal partners [
68
,
71
,
87
]. Conversely, parasitic behaviors of the fungus
can be observed in interaction with nonlichenized algae or lichenized algae from different
lichen species [
68
,
71
,
87
,
88
]. Switching to parasitism and saprotrophic nutrition is also
known in some lichens, like Ochrolechia frigida when growing without its alga partner. In
algal-free stages, this species seems to be capable of saprotrophic nutrition on mosses,
phanerogams and other lichens [89].
In agreement with an optional parasitic or saprotrophic lifestyle of the mycobiont,
Munzi et al. recorded for the first time in lichens a high activity of extracellular enzymes
able to digest organic matter of different types and that are usually found in mycorrhizal
fungi, which also alternate between different lifestyles (unpublished). A common charac-
teristic of axenic reconstitutions is either that they do not progress beyond the soredia or
squamule stages or, if they do, the resulting thalli do not resemble closely the corresponding
natural lichens in shape, size, and full differentiation. Gene expression studies [
72
] and
specific exudation patterns of lichen photobionts [
90
] also point to extracellular commu-
nication between lichen symbionts without cellular contact [
57
]. For example, ribitol was
capable of overcoming fungal growth arrest [
90
], fungal lectins induced chemotropism
of compatible Nostoc cells in cyanolichens [
91
], and chitinase, a defense enzyme in plants
against pathogens, was downregulated in the photobiont during resynthesis stages [
87
].
Interestingly, the results of proteomic analyses in the thalli of the lichen Xanthoria pari-
etina [
92
] included expression of proteins linked to the signaling compound pathways
mentioned above.
Our knowledge about the cytological and biochemical interactions between the sym-
bionts in lichens is still scarce [
88
]. However, increasing evidence indicates conservation of
signaling pathways involved in the establishment of other major symbioses between plants
and mutualistic microbes. Both common effectors and genes have been found to be essential
for the establishment of rhizobial, Frankia, mycorrhizal and fungal endophytic symbioses,
including plant-produced strigolactones, microbial partner-produced chitooligosaccharides
(COs) and lipo-chitooligosaccharides (LCOs) [
93
99
], genes encoding Vapyrin [
93
,
100
,
101
]
and several transcription factors [
102
,
103
]. Three of these transcription factors (CYCLOPS,
NSP1, and NSP2) are well conserved between actinorhizal, legume, non-legume, and
mycorrhizal symbioses [
96
]. It is therefore possible that some or all these factors are also
present and play essential roles in lichenization, and their absence or differential presence
may relate to re-synthesis failures or establishment of associations with parasitic outcomes.
Encyclopedia 2022,21428
6. Conclusions and Prospects
A large scientific effort is still needed to achieve the goal of revealing the physio-
logical mechanisms operating in convoluted lichen symbioses and the roles of the various
organisms involved in this complex holobiont. As the latest scientific evidence has shown,
this research challenge must be addressed by considering lichens as self-sustained and
adaptable systems of partnerships, just like us!
Author Contributions:
Conceptualization, S.M. and L.M.; methodology, S.M. and L.M.; software,
J.R.; validation, S.M., L.M., J.R. and C.C.; formal analysis, J.R.; investigation, L.M.; resources, C.C.,
L.M. and S.M.; data curation, L.M. and J.R.; writing—original draft preparation, L.M., J.R. and S.M.;
writing—review and editing, S.M., L.M., J.R. and C.C.; visualization, L.M. and J.R.; supervision, C.C.
and S.M.; project administration, L.M.; funding acquisition, L.M. All authors have read and agreed to
the published version of the manuscript.
Funding:
This project has received funding from the European Union’s Horizon 2020 Research
and Innovation programme under the Marie Skłodowska–Curie grant agreement #793965 (Med-
N-Change).
Acknowledgments: We are grateful to Lucy Sheppard for language revision and useful insights.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
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... These organisms are a symbiotic association between a fungus and an alga or a cyanobacterium. The fungus provides structure and protection, while the photosynthetic partner produces nutrients through photosynthesis [7]. Crustose lichens are characterized by their flattened, crust-like growth form that adheres tightly to the substrate. ...
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Tropical dry forests (TDFs) are unique ecosystems with high biodiversity, including a rich variety of lichen species. Lichens are sensitive to environmental changes and can serve as bioindicators of ecosystem health. This study examined the diversity of lichen communities at four TDF sites in the Atlántico Department of Colombia. More than 700 tree lichen specimens were collected and identified at the four sites. A total of 135 species of lichens were identified, of which 19 are possibly undescribed. The most diverse sites were Usiacurí and Repelón, both protected areas with relatively well-preserved forests. The findings of this study demonstrate that the Atlántico TDFs host a large diversity of lichens, with a significant number of records of new species. The observed differences in species composition between sites highlight the importance of habitat heterogeneity and anthropogenic pressures on lichen communities. The results emphasize the need for conservation strategies to protect these ecologically valuable lichen communities within the Atlántico TDFs.
... It represents more than 90 % of the lichen biomass. Within the lichen thalli, several algae species, yeasts, and even viruses have all been gradually found (Morillas et al., 2022). ...
... It represents more than 90 % of the lichen biomass. Within the lichen thalli, several algae species, yeasts, and even viruses have all been gradually found (Morillas et al., 2022). ...
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Thanks to their ability to absorb large amounts of trace elements from the atmosphere, lichens are widely used as bioaccumulators and bioindicators of air pollution. Among air pollutants, heavy metals represented by lead are the most important contributors to the deterioration of ecosystems. Fluorine is prevalent in a wide range of environmental matrices, even in trace amounts, and is one of the most phytotoxic halogens to plants. When lichens are exposed to air pollution, they frequently undergo structural, morphological and physiological alterations, and exhibit several coping strategies to combat and tolerate stressful situations. This manuscript presents general information about lichens, fluorine, and lead as well as the toxic effect of these two air pollutants on lichens, and the means of combat used by lichens to respond to fluorine and lead-induced stress.
... Lichens have shown their existence in a symbiotic association, established as composite organisms comprised of algae or cyanobacteria hosted by fungi. [2] The term 'lichen' is derived from the Ancient Greek word 'leikhen' , meaning 'which eats around itself ' , [3] and is also used in the context of 'warts' . [4] Another Greek word 'leprous' has been used in correlation with lichens recommending the utilization of lichens in alleviating skin diseases due to their peeling skin appearance. ...
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Over the past few decades, the rise in anthropogenic activities has led to environmental pollution. Heavy metals and metalloids like lead, arsenic, cadmium, mercury and aluminium are major pollutants hampering the harmony of the ecosystem. Biomonitoring describes various techniques and approaches for studying biological responses to pollution. The use of lichens in pollution monitoring proved to be an efficient method to curtail it. Representing a complex life form, lichens exist in a symbiotic association connecting algae and fungus. These biosensors are not only used to monitor environmental pollutants but have also been used medicinally since time immemorial. Lichens from Parmelia emerge as a valuable tool for monitoring pollution due to their unique capacity to accumulate heavy metals. Parmelia sulcata Taylor commonly known as shield lichen inhabited on trees, rocks and even on walls and is well distributed throughout the world from cold to temperate regions of the Northern and Southern hemispheres. For centuries, Parmelia sulcata has been used in traditional medicine to cure cranial disorders and also rubbed on the gums of teething babies to alleviate discomfort. It has been found that this lichen constitutes distinctive chemical constituents such as salazinic acid, atranorin, volatile oils, etc. contributing towards the anticancer, antioxidant, anti-microbial, anti-fungal and mosquitocidal potential. The prime objective of this current manuscript is to discuss the biomonitoring and pharmacological potential of Parmelia sulcata Taylor.
Chapter
This chapter aims at a comprehensive exploration of lichens, spanning their historical and contemporary applications in the realms of medicine and agriculture. It delves deeply into the intricate chemistry underpinning their antimicrobial properties, shedding light on current research endeavors aimed at unlocking the latent potential inherent in these often-overlooked organisms. The unfolding narrative reveals a compelling confluence of ancient knowledge and contemporary scientific pursuits, all geared toward the perpetual struggle against microbial adversaries. Lichens emerge as a prominent reservoir of secondary metabolites, prominently displaying a wide spectrum of antimicrobial activities. Notably, various lichen species including Alectoria sarmentosa , Bryoria fuscescens , Cetraria pinastri , Cladonia digitata , Cladonia fimbriate , Evernia divaricata , Lecanora frustulosa , Ochrolechia parella , Parmeliopsis hyperopta , Platismatia glauca , and Ramalina farinacea have exhibited substantial potential in combatting diverse microorganisms. Their relevance extends from historical medicinal practices to contemporary scientific investigations, reinforcing lichens as a promising frontier in the development of novel antimicrobial agents within the persistent endeavor to counteract microbial infections.
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Banyaknya air limbah domestik tanpa pengolahan terlebih dahulu dibuang ke air badan air sehingga dirasa semakin hari kualitas menjadi menurun. Kandungan organik dan mikroorganisme menjadi perhatian dalam segi kualitas. Tingginya kandungan organik dan mikrooorganisme seperti Total coliform. Penurunan parameter tersebut sebagai tujuan utama dalam penelitian ini. Pada proses aerob, pengolahan organik menggunakan pasokan udara sebesar 20 L/menit pada pengolahan secara tersuspensi dan terlekat untuk media terlekat menggunakan media kaldnes K5 dan bioball berduri masing-masing 30 % dari volume reaktor yang didahuili proses seeding dan aklimatisas. Variasi waktu pengolahan yang digunakan adalah tersuspensi 2 jam dan terlekat selama 6 jam serta sebaliknya. Selanjutnya diolah dengan pengolahan secara fisik secara simultan yakni proses pengendapan dan sterilisasi dengan waktu paparan dan pengendapan yakni 2 hingga 6 jam. Berdasarkan hasil penelitian menunjukkan hasil seeding dan aklimatisasi dilakukan selama 21 hari. Didapatkan pengolahan terbaik menggunakan tersuspensi 2 jam, terlekat 6 jam pada media kaldnes K5 dan pengendapan sekaligus paparan sinar ultraviolet selama 6 jam menunjukkan hasil penurunan COD sebesar 92,85 % dan untuk Total coliform sebesar 98,67 %. Kata Kunci: domestik, organik, media, ultraviolet
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Lichens represent self-supporting symbioses, which occur in a wide range of terrestrial habitats and which contribute significantly to mineral cycling and energy flow at a global scale. Lichens usually grow much slower than higher plants. Nevertheless, lichens can contribute substantially to biomass production. This review focuses on the lichen symbiosis in general and especially on the model species Lobaria pulmonaria L. Hoffm., which is a large foliose lichen that occurs worldwide on tree trunks in undisturbed forests with long ecological continuity. In comparison to many other lichens, L . pulmonaria is less tolerant to desiccation and highly sensitive to air pollution. The name-giving mycobiont (belonging to the Ascomycota), provides a protective layer covering a layer of the green-algal photobiont ( Dictyochloropsis reticulata ) and interspersed cyanobacterial cell clusters ( Nostoc spec.). Recently performed metaproteome analyses confirm the partition of functions in lichen partnerships. The ample functional diversity of the mycobiont contrasts the predominant function of the photobiont in production (and secretion) of energy-rich carbohydrates, and the cyanobiont’s contribution by nitrogen fixation. In addition, high throughput and state-of-the-art metagenomics and community fingerprinting, metatranscriptomics, and MS-based metaproteomics identify the bacterial community present on L. pulmonaria as a surprisingly abundant and structurally integrated element of the lichen symbiosis. Comparative metaproteome analyses of lichens from different sampling sites suggest the presence of a relatively stable core microbiome and a sampling site-specific portion of the microbiome. Moreover, these studies indicate how the microbiota may contribute to the symbiotic system, to improve its health, growth and fitness.
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The diversity of lichen-associated bacteria from lichen taxa Cetraria, Cladonia, Megaspora, Pseudephebe, Psoroma, and Sphaerophorus was investigated by sequencing of 16S rRNA gene amplicons. Physiological characteristics of the cultured bacterial isolates were investigated to understand possible roles in the lichen ecosystem. Proteobacteria (with a relative abundance of 69.7–96.7%) were mostly represented by the order Rhodospirillales. The 117 retrieved isolates were grouped into 35 phylotypes of the phyla Actinobacteria (27), Bacteroidetes (6), Deinococcus-Thermus (1), and Proteobacteria (Alphaproteobacteria (53), Betaproteobacteria (18), and Gammaproteobacteria (12)). Hydrolysis of macromolecules such as skim milk, polymer, and (hypo)xanthine, solubilization of inorganic phosphate, production of phytohormone indole-3-acetic acid, and fixation of atmospheric nitrogen were observed in different taxa. The potential phototrophy of the strains of the genus Polymorphobacter which were cultivated from a lichen for the first time was revealed by the presence of genes involved in photosynthesis. Altogether, the physiological characteristics of diverse bacterial taxa from Antarctic lichens are considered to imply significant roles of lichen-associated bacteria to allow lichens to be tolerant or competitive in the harsh Antarctic environment.
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Short chain chitooligosaccharides (COs) are chitin derivative molecules involved in plant-fungus signaling during arbuscular mycorrhizal (AM) interactions. In host plants, COs activate a symbiotic signalling pathway that regulates AM-related gene expression. Furthermore, exogenous CO application was shown to promote AM establishment, with a major interest for agricultural applications of AM fungi as biofertilizers. Currently, the main source of commercial COs is from the shrimp processing industry, but purification costs and environmental concerns limit the convenience of this approach. In an attempt to find a low cost and low impact alternative, this work aimed to isolate, characterize and test the bioactivity of COs from selected strains of phylogenetically distant filamentous fungi: Pleurotus ostreatus, Cunninghamella bertholletiae and Trichoderma viride. Our optimized protocol successfully isolated short chain COs from lyophilized fungal biomass. Fungal COs were more acetylated and displayed a higher biological activity compared to shrimp-derived COs, a feature that—alongside low production costs—opens promising perspectives for the large scale use of COs in agriculture.
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Multi-omics, variously called integrated omics, pan-omics, and trans-omics, aims to combine two or more omics data sets to aid in data analysis, visualization and interpretation to determine the mechanism of a biological process. Multi-omics efforts have taken center stage in biomedical research leading to the development of new insights into biological events and processes. However, the mushrooming of a myriad of tools, datasets, and approaches tends to inundate the literature and overwhelm researchers new to the field. The aims of this review are to provide an overview of the current state of the field, inform on available reliable resources, discuss the application of statistics and machine/deep learning in multi-omics analyses, discuss findable, accessible, interoperable, reusable (FAIR) research, and point to best practices in benchmarking. Thus, we provide guidance to interested users of the domain by addressing challenges of the underlying biology, giving an overview of the available toolset, addressing common pitfalls, and acknowledging current methods’ limitations. We conclude with practical advice and recommendations on software engineering and reproducibility practices to share a comprehensive awareness with new researchers in multi-omics for end-to-end workflow.
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Background: Symbiosis is central to ecosystems and has been an important driving force of the diversity of life. Close and long-term interactions are known to develop cooperative molecular mechanisms between the symbiotic partners and have often given them new functions as symbiotic entities. In lichen symbiosis, mutualistic relationships between lichen-forming fungi and algae and/or cyanobacteria produce unique features that make lichens adaptive to a wide range of environments. Although the morphological, physiological, and ecological uniqueness of lichens has been described for more than a century, the genetic mechanisms underlying this symbiosis are still poorly known. Results: This study investigated the fungal-algal interaction specific to the lichen symbiosis using Usnea hakonensis as a model system. The whole genome of U. hakonensis, the fungal partner, was sequenced by using a culture isolated from a natural lichen thallus. Isolated cultures of the fungal and the algal partners were co-cultured in vitro for 3 months, and thalli were successfully resynthesized as visible protrusions. Transcriptomes of resynthesized and natural thalli (symbiotic states) were compared to that of isolated cultures (non-symbiotic state). Sets of fungal and algal genes up-regulated in both symbiotic states were identified as symbiosis-related genes. Conclusion: From predicted functions of these genes, we identified genetic association with two key features fundamental to the symbiotic lifestyle in lichens. The first is establishment of a fungal symbiotic interface: (a) modification of cell walls at fungal-algal contact sites; and (b) production of a hydrophobic layer that ensheaths fungal and algal cells;. The second is symbiosis-specific nutrient flow: (a) the algal supply of photosynthetic product to the fungus; and (b) the fungal supply of phosphorous and nitrogen compounds to the alga. Since both features are widespread among lichens, our result may indicate important facets of the genetic basis of the lichen symbiosis.
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This study analyses the interactions among crustose and lichenicolous lichens growing on gypsum biocrusts. The selected community was composed of Acarospora nodulosa, Acarospora placodiiformis, Diploschistes diacapsis, Rhizocarpon malenconianum and Diplotomma rivas-martinezii. These species represent an optimal system for investigating the strategies used to share phycobionts because Acarospora spp. are parasites of D. diacapsis during their first growth stages, while in mature stages, they can develop independently. R. malenconianum is an obligate lichenicolous lichen on D. diacapsis, and D. rivas-martinezii occurs physically close to D. diacapsis. Microalgal diversity was studied by Sanger sequencing and 454-pyrosequencing of the nrITS region, and the microalgae were characterized ultrastructurally. Mycobionts were studied by performing phylogenetic analyses. Mineralogical and macro- and micro-element patterns were analysed to evaluate their influence on the microalgal pool available in the substrate. The intrathalline coexistence of various microalgal lineages was confirmed in all mycobionts. D. diacapsis was confirmed as an algal donor, and the associated lichenicolous lichens acquired their phycobionts in two ways: maintenance of the hosts’ microalgae and algal switching. Fe and Sr were the most abundant microelements in the substrates but no significant relationship was found with the microalgal diversity. The range of associated phycobionts are influenced by thallus morphology.
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This article is a Commentary on Mark et al. (2020), 227: 1362–1375.
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Symbiotic associations between endophytic fungi, hereon referred to as mycoendophytes, and their hosts involve several metabolic and regulatory processes. The exact molecular signal mechanisms that underlie these interactions are largely unidentified. Nevertheless, phytohormones seem to play key roles in the establishment and perpetuation of these symbiotic associations including plant-mycoendophyte symbiosis. Strigolactones, a group of apocarotenoid phytohormones, are known to influence both plant and fungal developmental processes e.g. modulation of host-root parasitic plant interactions and the activation of hyphae growth and branching. However, their role in plant-mycoendophyte interactions remains largely undescribed. Here, we provide a concise synthesis of current scientific knowledge on strigolactone influences in shaping plant-mycoendophyte symbiotic interactions, while also providing some perspective and research directions on critical molecular, physiological and ecological aspects that hold promise to deepen our understanding of this biologically and ecologically significant interaction.
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The frequent discrepancy between direct microscopic counts and numbers of culturable bacteria from environmental samples is just one of several indications that we currently know only a minor part of the diversity of microorganisms in nature. A combination of direct retrieval of rRNA sequences and whole-cell oligonucleotide probing can be used to detect specific rRNA sequences of uncultured bacteria in natural samples and to microscopically identify individual cells. Studies have been performed with microbial assemblages of various complexities ranging from simple two-component bacterial endosymbiotic associations to multispecies enrichments containing magnetotactic bacteria to highly complex marine and soil communities. Phylogenetic analysis of the retrieved rRNA sequence of an uncultured microorganism reveals its closest culturable relatives and may, together with information on the physicochemical conditions of its natural habitat, facilitate more directed cultivation attempts. For the analysis of complex communities such as multispecies biofilms and activated-sludge flocs, a different approach has proven advantageous. Sets of probes specific to different taxonomic levels are applied consecutively beginning with the more general and ending with the more specific (a hierarchical top-to-bottom approach), thereby generating increasingly precise information on the structure of the community. Not only do rRNA-targeted whole-cell hybridizations yield data on cell morphology, specific cell counts, and in situ distributions of defined phylogenetic groups, but also the strength of the hybridization signal reflects the cellular rRNA content of individual cells. From the signal strength conferred by a specific probe, in situ growth rates and activities of individual cells might be estimated for known species. In many ecosystems, low cellular rRNA content and/or limited cell permeability, combined with background fluorescence, hinders in situ identification of autochthonous populations. Approaches to circumvent these problems are discussed in detail.
Book
This book compiles various methodologies used in understanding interactions within the rhizosphere. An in-depth understanding of the rhizosphere is essential to developing successful strategies for future sustainable agriculture. The book summarizes methods and techniques used to study the mechanisms involved in mutualistic symbioses and pathogenic interactions of plants with various microbial organisms including fungi, bacteria, and oomycetes. Each chapter discusses different methodologies used in rhizosphere biology, while also providing real-world experimental data and trouble-shooting tips. Interested researchers will also find a wealth of literature references for further research. As the first comprehensive manual and compilation of methods and techniques used in rhizosphere biology, the book represents an essential resource for all researchers who are newcomers to soil microbiology experimentation.