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Lichens – life in extreme conditions

British Lichen Society

Pat Wolseley

Rough outline of talk

• Where to find lichens• What is a lichen, mainly about ascomycetes• Fungal reproduction, photobiont and thallus

structure• New insights, molecular and others• Lichen chemistry• New organisms and techniques• Adaptations to a changing environment

A rocky shore – tolerant of salt water, high temperatures and UV, and high nitrogen from sea birds.

Skomer island in Pembrokeshire

The grey lichen below is Ramalina siliquosa and the yellow lichen is Xanthoria parietina – abundant on bird cliffs and also common inland on farm rooves.

Where do we find lichens?

In a desert -

Crustose lichens growing on rocks in the Sierra Nevada

Bright colours produced by fungus as sunscreen to protect algal partner against heat and UV.

High altitudes and polar regions

e.g. Britain at the end of the last ice-age c. 10,000 years ago

Cold and frequently covered in snow and ice. High UV when exposed.

Hot and wet in a Tropical Rainforest in Thailand

Conditions similar to Britain in the tertiary period 70 million years ago.

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A tropical forest or a wet day in a Celtic rain forest?Lichens on rocks as well as trees c.400 species in 36 ha!

In our towns and gardensOn our garden trees where moisture, light and nutrients are plentiful.

On a roof which may be hot and dry or soaking wet!

On pavements – the ‘chewing gum’ lichen prefers the concrete to the brick picture by Alan Silverside

What is a Lichen?

• Fungus (mycobiont) and alga or cyanobacteria (photobiont)

• Symbiotic or Parasitic?• Photobiont: provides food

but does not reproduce sexually in a lichen

• Mycobiont: protection and body shape, sexual reproduction by spores

• Successful relationship: ‘extremophiles’

Schwendener in 1867 looked down a microscope and suggested that lichens are dual organisms with algae and cyanobacteria

a community of two or more organisms

20% of all known fungi lichenized mainly in two orders Ascomycetes and Basidiomycetes

Basidiomycetes

gill and bracket fungi with spores borne on a basidium

Bracket fungi

Tropical basidiomycete

Dictyonema sp.

Gill fungi lichenised

Omphalina umbelliferae

Orange peel cup fungus

Coenogonium luteum - crustose lichen with yellow fruiting bodies

Lobaria pulmonaria tree lungwort with brown fruiting bodies

Ascomycete fruiting bodies

Ascomycetes –spore production

apothecium

hymenium

hypothecium

Lecanorine apothecia –exciple same as thallus

Lecideine apothecia – exciple unlike thallus

Spores produced in an ascus in an apothecium

Lecidella elaeochroma

Physcia aipolia

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Apothecia come in many shapes and sizes

Arthonia radiata –irregular lirellae

Graphis scripta

Star-like fruiting bodies without raised margins

Graphidaceae with raised lip-like margins

Pyrenula macrospora

Pyrenula nitidella

Spores in a carbonised perithecium spores released through a pore-like ostiole

Pyrenulaceae

Lichens – growth form & shape

branched & shrub-like, attached at the base only

leaf-like lobes, closely or loosely attached to the

substrate from the lower surface

with the entire lower surface closely attached

to the substrate

crustosefoliosefruticose

Which photobionts found in lichens?Green single-celled algae Trebouxia rarely found free-living.

Yellowish Trentepohlia filamentous algae -free-living in warm conditions.

Blue-green cyanobacteriaNostoc fixes nitrogen.

Unlike this free-living green alga Desmococcuscommon everywhere.

Photobiont

Trebouxia a green single celled chlorococcoid alga

Lichen orders

Peltigerales

Thallus grey when wet

Lecanorales, Pertusariales

Thallus green when wet

Arthoniales, Graphidales

Thallus yellow when scratched

Nostoc and other cyanobacteria that fix nitrogen

Relationship of phycobionts to lichen orders

Trentepohlia a yellow filamentous chlorococcoid alga (not always appearing filamentous in lichens)

Thallus structure

cortex

medulla

lower cortex

homoiomerousheteromerous

filamentous

Lower cortex

cyphella

pseudocyphella

photobiont

photobiont

Parmotrema perlatum heteromerous with dark lower surface

Leptogium cyanescens –homiomerous with cyanobacterial photobiont

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Molecular insights into Stictis species

Stictis - a genus of saprotrophic fungi growing on decorticated bark of poplar twig

Conotrema –lichenised fungus growing on old bark of poplar

Fruitbody of Conotrema showing lichenised thallus

Molecular cladogram showing that 3 species of Conotrema & Stictis have optional lifestyles

Result – Conotrema spp. included in Stictis (the older name)

Wedin, M. et al. 2004: Saprotrophy and lichenization as options for the same fungal species on different substrata: enzironmental plasticity and fungal lifestyles in the Stictis-Conotrema complex. - New Phytologist164: 459-465.

Is lichenisation optional for a fungus?

Same fungus given two names with different photobionts

James, PW/ Henssen, A 1976: The morphological and taxonomic significance of cephalodia. - In: D. H. Brown, D. L. Hawksworth & R. H. Bailey (eds.): Lichenology: Progress and Problems. Academic Press, London, pp. 27-77.

Sticta dufourii sens lat –cyanobacterial morph

Sticta canariensis - green morph

Adaptation to different photobionts

Two or more photobiontsCephalodia - internal

Or external

Same fungus Lobaria amplissima with cyanobacterial photobiont and thallus changes morphology from foliose to fruticose.

trebouxia

cyanobacteria

Cephalodia in Peltigera sp

How does a symbiotic organism reproduce itself?A germinating fungal spore must find the right algal partner?

The alternative - distribute both partners together as propagules

Granular particles of a mixture of algae and fungus called soredia

Possibilities of a propagule?

Belinchón, R./ Yahr, R./ Ellis, C.J. 2015: Interactions among species with contrasting dispersal modes explain distributions for epiphytic lichens. - Ecography 38(8): 762–768.

Possibilities of a propagule?• Propagules growing into independent lichen thalli• Many propagules from different thalli growing together and producing one

organism• Propagules from one organism raided by another for the photobiont

A Scottish survival story – Nephroma laevigatum and N. parile have the same cyanobacterial photobiont

Nephroma laevigatum with spore producing apothecia and no soredia

Nephroma parile with soredia and no apothecia

Result: co-dependence of the more sensitive N. laevigatum with asexual and more frequent N.parile.

Lichen ChemistrySecondary compounds formed by the mycobiont

situated in cortex or medulla

protection against extreme UV, high moisture and drought, predation, pollution .

Xanthoria parietina – anthraquinones (KOH + purple) in medullaSpot tests for

compoundsFirst used as a taxonomic tool by Nylander in 1850’s

Standard tests:•10% KOH (K)•Thin Bleach (C)• p-phenylenediamine (P)

Parmelinella wallichiana

KOH + red

Salazinic acid

Rikkinen, J 1995: What's behind the pretty colours? A study on the photobiology of lichens. - Bryobrothera 4: 1-239.

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Location of secondary metabolites

SEM Photograph by R. Honegger

As crystals around the hyphae in the medulla and/or the cortexOn the spore bearing tissue

More than 700 compounds identified in lichenssource of pharmaceutically valuable compounds

Detection of secondary compounds Thin layer chromatography (TLC) in 2 different solvents

Control atranorin

norstictic

Usnic acid

Fumarprotocetraric acid

Results of TLC of sterile crust species of Lepraria

Discovery of another organism in lichens in 2015

In the USA two Bryoria species with different chemistry but no other morphological differences were discovered to have live yeast cells in one species C & D and not in the other A & B

http://www.theatlantic.com/science/archive/2016/07/how-a-guy-from-a-montana-trailer-park-upturned-150-years-of-biology/491702/

See Spribille story in:

Fluorescent cell imaging of fungal elements in an SEM of a thallus filament (A) of Bryoria capillarisB - showing yeasts (green), lichen hyphae (blue) and trebouxia photobiont (red)C- detail of yeast cells

Location of components in a Bryoria thallus

Since the first discovery Spribille & team have shown that yeasts are widespread in most lichens!

morphology

ascus structure

thallus structure

chemistry

DNA structure

Barcoding a community?

naked eye and hand lens

microscope

Molecular analysis

microscope, SEM

TLC, HPTLC, HPLC

Taxonomic tools

Acharius 1790’s

Culberson 1960’s - Elix

Hale – 1970s Vobis

Hafellner 1984

Blum 1986 -present

Adaptations to a changing environment

• Disappearing landscapes: veteran trees and woodpasture along with their indicator species.

• Climate change - are Mediterranean species coming in and sensitive species disappearing?

• Urban and agricultural pollution; switch from acid rain to Nitrogen. Look at our cities lichens everywhere but which ones?

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Lobaria pulmonaria – tree lungwort

• air pollution sensitive

• Large foliose indicator of bryo-lichen community

Indicators of ecological continuity

Lichens as indicators of environmental continuity in Somerset

Aerial view of Horner woods NNR. 358 lichens recorded including 45/70 indicators of environmental continuity.

Lungwort - Lobaria pulmonaria the classic indicator of ancient woodlands.

Lobaria pulmonaria in Horner 1970 to 2012Francis Rose surveys in 1974 to 1984 stated Lobaria seen on c. 300 trees

Lobaria pulmonaria in upper Horner valleys in 2012 – 44 trees with Lobaria recorded (Sanderson 2012)

Lobaria pulmonaria in Horner valleys in 1988 on 166 trees – on 62 trees in blue square (Wolseley & O’Dare Exmoor woodland survey

Lobaria in a changing Somerset landscape

1886 ordnance survey of woodlands and parkland at Nettlecombe

Lobaria pulmonaria in 2005 on veteran trees several hundred years old grown in very different conditions

Disjunct distributions – UK and tropics?

Pseudocyphellaria crocata – gold spot lichen rare on ash trees in Barle valley

Kinabalu mountain in BorneoThe same lichen is abundant on trees at c. 4,000 m in Borneo

Usnea florida recorded as common on trunks and branches of trees in 1930 (Watson)

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Climate change - increasing average temp and longer dry periods

Mediterranean species increasing

Flavoparmelia soredians

1960-1999 2000 onwards

Nephroma arcticum in Norway is a conspicuous leafy species with large brown fruits.

Cool temperate species disappearing

N. arcticum now a scruffy infertile species rare in alpine heaths in the Cairngorms

Conservation project to protect it from grazers with wire baskets.

The urban landscape

• Decreasing SO2, increasing Nitrogen mainly as NO2• Increasing dust and particulates - increased bark pH• Increasing warmth from different sources

The rural landscape

• Increasing N as ammonia NH3• Increasing arable and dust

N-tolerant (nitrophytes)N-sensitive ( nitrophobes)

• Involve public in England in collecting data on common easy to ID species that can be used as indicators of air quality.

• Select 3 N-tolerant and 3-N sensitive, & 3 intermediate taxa.

• Produce fold out and workbook

• Survey data entered onlinehttp://www.opalexplorenature.org/

• Pollution index using total N sensitive species minus total N tolerant species using cover value of 1-3

Usnea spp.

Evernia prunastri

Hypogymnia spp.

Xanthoria parietina

Xanthoria polycarpa

Physcia tenella /P.adscendens

Lottery funded OPAL methodology

N pollution score across England

-23 to -54 N-tolerant species dominant – mainly in rural areas with intensive agriculture

0 to-22 N-tolerant species frequent – in urban areas throughout

1 to 22 N-sensitive lichens present N-tolerant spp. may be present –widely distributed in rural and urban areas

23 to54 N-sensitive lichens dominant – only found in unpolluted sites or where ID mistaken!

Note very few surveys undertaken in nature reserves.

abundance x diversity weighted indicator spp. score - data from all trees