A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens

Lendemer, James C.; Keepers, Kyle G.; Tripp, Erin A.; Pogoda, Cloe S.; McCain, Christy M.; Kane, Nolan C.

doi:10.1002/ajb2.1339

Cited by 35 publications

(23 citation statements)

References 49 publications

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“…L a t e r Č e r n a j o v á a n d Š k a l o u d ( 2 0 1 9 ) f o u n d Cystobasidiomycete yeasts in 95% of Cladonia specimens collected across Europe, though they were suggested to be either part of a superficial biofilm or living within the thallus without associating with the cortex itself. In contrast, Lendemer et al (2019) found them in just nine of the 339 species investigated. The question remains of how abundant and specific cystobasidiomycetes are in lichen symbioses, as well as how consistent the mycobiome might be among different lichen-forming fungal species, e.g., do evolutionary constraints of the mycobiont influence the range and composition of associated fungi?…”

Section: Introductionmentioning

confidence: 86%

Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

et al. 2020

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Lichens have traditionally been considered the symbiotic phenotype from the interactions of a single fungal partner and one or few photosynthetic partners. However, lichen symbioses have been shown to be far more complex and may include a wider range of other interacting organisms, including non-photosynthetic bacteria, accessory fungi, and algae. In this study, we analyzed metagenomic shotgun sequences in an attempt to characterize lichen mycobiomes. Specifically, we inferred the range of fungi associated within lichen thalli from five groups of lichenshorsehair lichens (mycobiont = Bryoria spp.), shadow lichens (taxa in Physciaceae), rock posies (Rhizoplaca spp.), rock tripes (Umbilicaria spp.), and green rock shields (Xanthoparmelia spp.). Metagenomic reads from the multi-copy nuclear ribosomal internal transcribed spacer region, the standard DNA barcode region for fungi, were extracted, clustered, and used to infer taxonomic assignments. Our data revealed diverse lichen-associated mycobiomes. Many of the members of the lichen-associated mycobiomes that were identified here have not previously been found in association with lichens. Furthermore, closely related mycobionts tended to have more similar mycobiomes. We found little evidence supporting the ubiquitous presence of Cystobasidiales yeasts in macrolichens, although reads representing this putative symbiotic partner were found in samples of Bryoria lichens, albeit in low abundance. Our study further highlights the ecosystem-like features of lichens, with partners and interactions far from being completely understood. Future research is needed to more fully and accurately characterize lichen mycobiomes and how these fungi interact with the major lichen components, the photo-and mycobionts.

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Section: Introductionmentioning

confidence: 86%

Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

et al. 2020

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“…The mycobiont-photobiont studies focused exclusively on New Zealand (Buckley et al 2014;Rafat et al 2015) and Antarctica (Park et al 2014(Park et al , 2015. The third major group of accessions (11%) originated from floristic and (meta-)barcoding surveys (Hur et al 2005;Kim et al 2006;Kelly et al 2011;Orock et al 2012;Schoch et al 2012;Šoun et al 2015;Mark et al 2016b;Jaouen et al 2019;Lendemer et al 2019;Marthinsen et al 2019).…”

Section: Metadata Diversitymentioning

confidence: 99%

“…is defined as a shrubby, sorediate taxon with inflated branches constricted at their point of attachment, minute soralia producing isidiomorphs along the terminal branches, but the taxon was described as highly variable both morphologically and in the medullary chemistry (Clerc 2007;Randlane et al 2009;Gerlach et al 2019aGerlach et al , 2020. It has been reported from all major regions and is considered presumably subcosmopolitan (Awasthi 1986;Clerc 1987Clerc , 2004Clerc , 2006Clerc , 2007Clerc , 2011bMarcano et al 1996;Clerc & Herrera-Campos 1997;Halonen et al 1998;Elix & McCarthy 1998Fos & Clerc 2000;Herrera-Campos et al 2001;Galloway 2007;Hinds & Hinds 2007;Randlane et al 2009;Smith et al 2009;Kelly et al 2011;Rodriguez et al 2011a;Saag et al 2011;Ohmura 2012;Schoch et al 2012;Noer et al 2013;Santiago et al 2013;Truong et al 2013a;Millanes et al 2014;Araujo 2016, as Gerlach et al 2019a;Lendemer et al 2019;Lücking et al 2020c). Truong et al (2013a) first demonstrated that U. cornuta s.lat.…”

Section: Usnea Subgenus Neuropogon New Zealand Cladementioning

confidence: 99%

Two decades of DNA barcoding in the genus Usnea (Parmeliaceae): how useful and reliable is the ITS?

Lücking¹,

Nadel²,

Araújo³

et al. 2020

Plant and Fungal Systematics

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We present an exhaustive analysis of the ITS barcoding marker in the genus Usnea s.lat., separated into Dolichousnea, Eumitria, and Usnea including the subgenus Neuropogon, analyzing 1,751 accessions. We found only a few low-quality accessions, whereas information on voucher specimens and accuracy and precision of identifications was of subpar quality for many accessions. We provide an updated voucher table, alignment and phylogenetic tree to facilitate DNA barcoding of Usnea, either locally or through curated databases such as UNITE. Taxonomic and geographic coverage was moderate: while Dolichousnea and subgenus Neuropogon were well-represented among ITS data, sampling for Eumitria and Usnea s.str. was sparse and biased towards certain lineages and geographic regions, such as Antarctica, Europe, and South America. North America, Africa, Asia and Oceania were undersampled. A peculiar situation arose with New Zealand, represented by a large amount of ITS accessions from across both major islands, but most of them left unidentified. The species pair Usnea antarctica vs. U. aurantiacoatra was the most sampled clade, including numerous ITS accessions from taxonomic and ecological studies. However, published analyses of highly resolved microsatellite and RADseq markers showed that ITS was not able to properly resolve the two species present in this complex. While lack of resolution appears to be an issue with ITS in recently evolving species complexes, we did not find evidence for gene duplication (paralogs) or hybridization for this marker. Comparison with other markers demonstrated that particularly IGS and RPB1 are useful to complement ITS-based phylogenies. Both IGS and RPB1 provided better backbone resolution and support than ITS; while IGS also showed better resolution and support at species level, RPB1 was less resolved and delineated for larger species complexes. The nuLSU was of limited use, providing neither resolution nor backbone support. The other three commonly employed protein-coding markers, TUB2, RPB2, and MCM7, showed variable evidence of possible gene duplication and paralog formation, particularly in the MCM7, and these markers should be used with care, especially in multimarker coalescence approaches. A substantial challenge was provided by difficult morphospecies that did not form coherent clades with ITS or other markers, suggesting various levels of cryptic speciation, the most notorious example being the U. cornuta complex. In these cases, the available data suggest that multimarker approaches using ITS, IGS and RPB1 help to assess distinct lineages. Overall, ITS was found to be a good first approximation to assess species delimitation and recognition in Usnea s.lat., as long as the data are carefully analyzed, and reference sequences are critically assessed and not taken at face value. In difficult groups, we recommend IGS as a secondary barcode marker, with the option to employ more resource-intensive approaches, such as RADseq, in species complexes involving so-called species pairs or other cases of disparate morphology not reflected in the ITS or IGS. Attempts should be made to close taxonomic and geographic gaps especially for the latter two markers, in particular in Eumitria and Usnea s.str. and in the highly diverse areas of North America and Central America, Africa, Asia, and Oceania.

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“…The significance of these lichen yeasts was discussed by the late Franz Oberwinkler (2017) who concluded that 'it is obvious that basidiomycetous yeasts in lichen thalli are not a third component of symbiosis, but rather the vegetative propagules of mycoparasites'. Moreover, a broad survey for basidiomycete yeasts through metagenomic analysis of 339 lichen species (of 25 orders) confirmed the yeasts in only 2.7% of the sampled species (Lendemer et al, 2019), although their metagenomic approach may be much less sensitive than PCR assays with specific primers. It remained, therefore, unclear, how ubiquitous and specific these yeast asexual stages actually were.…”

mentioning

confidence: 99%

Lichens redefined as complex ecosystems

2020

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A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens

Abstract: A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens.

Cited by 35 publications

References 49 publications

Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

Two decades of DNA barcoding in the genus Usnea (Parmeliaceae): how useful and reliable is the ITS?

Lichens redefined as complex ecosystems

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