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10/2/2018
1
Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment
John Taylor UC Berkeley
Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment
UC Berkeley, Northern Arizona University, TGen
John Taylor, Rachel Adams, Cheng Gao, Bridget Barker
10/2/2018
2
Basidiomycota - Cryptococcus
Ascomycota – Taphrinomycotina - Pneumocystis
Ascomycota – Saccharomycotina - Candida
Ascomycota – Pezizomycota – EurotiomycetesEurotiales - Aspergillus
Ascomycota – Pezizomycota – EurotiomycetesOnygenales – Endemic Mycoses
Where are the agents of endemic mycoses?
Basidiomycota - Cryptococcus
Ascomycota – Taphrinomycotina - Pneumocystis
Ascomycota – Saccharomycotina - Candida
Ascomycota – Pezizomycota – EurotiomycetesEurotiales - Aspergillus
Ascomycota – Pezizomycota – EurotiomycetesOnygenales – Endemic Mycoses
Where are the agents of endemic mycoses?
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CoccidioidesHistoplasmaBlastomyces
Paracoccidioides
Coccidioides
Muñoz et al. 2018. Scientific ReportsDOI:10.1038/s41598-018-22816-6
Onygenales
Aspergillus
CoccidioidesHistoplasmaBlastomyces
Paracoccidioides
Coccidioides
Muñoz et al. 2018. Scientific ReportsDOI:10.1038/s41598-018-22816-6
Onygenales
Aspergillus
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CoccidioidesHistoplasmaBlastomyces
Paracoccidioides
Coccidioides
Muñoz et al. 2018. Scientific ReportsDOI:10.1038/s41598-018-22816-6
Onygenales
Aspergillus
www.emedicine.com
Healthy Infected
What is coccidioidomycosis?
10/2/2018
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Distribution
of
Coccidioides
species
Hector and Laniado-Laborin
2005. PLoSMedicine
What is coccidioidomycosis and why should we care?
What is coccidioidomycosis and why should we care?
Arizona
California
https://www.cdc.gov/fungal/diseases/coccidioidomycosis/statistics.html
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6
2016
What is coccidioidomycosis and why should we care?
California
Cooksey et al. 2017 MMWR August 11, 2017 / 66(31);833–834
2017
What is coccidioidomycosis and why should we care?https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf
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Move from the patient to the environment.
Move from the patient to the environment.Diagnostics.
How dangerous is this job? Do I need a respirator?
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Move from the patient to the environment.Diagnostics.
How dangerous is this job? Do I need a respirator?Pharmaceuticals.
Is this area so dangerous that I need to take antifungals prophylactically?
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Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
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Background
Small mammals
Chester W. Emmons
1942
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Granuloma in mouse lung
Ashburn and Emmons 1942. Archives of Pathology 34:791-800.
1942
13%
17%
Emmons and Ashburn, 1942
1942
Pocket Mouse
Kangaroo Rat
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C. W. EMMONS
/
/
/
. . . it may be primarily a disease of rodents . . . certain species of rodents constitute a natural reservoir of coccidioidomycosis and by their geographical distribution determine the areas of endemicity of the disease.
1943
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Coccidioides immitis in the soil of the southern San Joaquin Valley.Roger O. Egeberg and Ann Frank Ely
American Journal of the Medical Sciences, February 1956, 151-41956
Coccidioides immitis in the soil of the southern San Joaquin Valley.Roger O. Egeberg and Ann Frank Ely
American Journal of the Medical Sciences, February 1956, 151-41956
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Growth patterns of Coccidioides immitis in the soil of an endemic area.Ann Frank Elconin, Roger O. Egeberg and Robert LubarskyIn: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.
Public Health Service Publication 575.
428 7.4%Total 31
1957
Growth patterns of Coccidioides immitis in the soil of an endemic area.Ann Frank Elconin, Roger O. Egeberg and Robert LubarskyIn: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.
Public Health Service Publication 575.
1957
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Growth patterns of Coccidioides immitis in the soil of an endemic area.Ann Frank Elconin, Roger O. Egeberg and Robert LubarskyIn: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.
Public Health Service Publication 575.
1957
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Ecological studies of Coccidioides immitis.Orda A. Plunkett and F. E. Swatek
In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.Public Health Service Publication 575.
1957
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.
Ecological studies of Coccidioides immitis.Orda A. Plunkett and F. E. Swatek
In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.Public Health Service Publication 575.
1957
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.
Soil Samples from the midden were positive.
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Ecological studies of Coccidioides immitis.Orda A. Plunkett and F. E. Swatek
In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.Public Health Service Publication 575.
1957
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.
Soil Samples from the midden were positive.
80 burrow samples taken near the midden – all negative.
Ecological studies of Coccidioides immitis.Orda A. Plunkett and F. E. Swatek
In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.Public Health Service Publication 575.
1957
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.
Soil Samples from the midden were positive.
80 burrow samples taken near the midden – all negative.
440 pocket mice and kangaroo rats captured near the midden -- all negative.
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Studies of physical parameters.
Climate: temperature, water and wind
Soil
1957-2018
Morbidity caused by C. immitis was best explained by the interactionbetween two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Climate: California
2000
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
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Morbidity caused by C. immitis was best explained by the interactionbetween two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Relative change in cocci
morbidity
Climate: California
2000
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
Morbidity caused by C. immitis was best explained by the interactionbetween two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Relative change in cocci
morbidity
Model based on length of drought and mean annual rainfall in the preceding year
Climate: California
2000
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
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GeoHealth 1, 51–63 (2017)
The results indicate that in both states, coccidioidomycosis incidence
is related to soil moisture levels from previous summers and falls.
Climate: California & Arizona
2017
ClimateSoil
Coccidioides
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ClimateSoil
Coccidioides
ClimateSoil
Coccidioides
Cocci has to eat.
10/2/2018
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Background
Fungal Nutrition
Ascomycota, Pezizomycotina
htt
p:/
/web
.sta
nfo
rd.e
du
/~si
egel
r/fu
ng
i/cr
amp
ba
ll.h
tml
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
de.wikipedia.org
10/2/2018
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Evolution of Gene Family Size
Sharpton, Stajich et al. 2009. Genome Research
2009
Eurotiales
Onygenales
Sordariomycetes
Sharpton, Stajich et al. 2009. Genome Research
Gene Family Reductions:
Genes coding enzymes
that digest plants
2009
https://www.123rf.com/photo_27279678_dried-out-dead-plants-lying-in-a-dry-arid-desert-environment.html
10/2/2018
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Keratin, hair, skin & connective tissue
www.privemillenia.com
Rock Pocket Mouse
http://www.snipview.com/q/Rock%20pocket%20mouse
Sharpton, Stajich et al. 2009. Genome Research
Gene Family Reductions:
Genes coding enzymes
that digest animals
2009
Jonah Evans, Texas. Parks and Wildlife Department, http://www.inaturalist.org/photos/407437
Perognathus longimembris
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Ascomycota, Pezizomycotina
htt
p:/
/web
.sta
nfo
rd.e
du
/~si
egel
r/fu
ng
i/cr
amp
ba
ll.h
tml
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
de.wikipedia.org
Ecology
Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.
10/2/2018
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Ascomycota, Pezizomycotina
htt
p:/
/web
.sta
nfo
rd.e
du
/~si
egel
r/fu
ng
i/cr
amp
ba
ll.h
tml
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
de.wikipedia.org
Ecology
Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.
Hypothesis, Coccidioides spp. are Endozoans, they live in their natural animal hosts without causing apparent disease. When the animal dies, the fungus becomes active, consumes the dead animal and reproduces.
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ClimateSoil
Coccidioides
Cocci has to eat.
ClimateSoil
Animal
Coccidioides
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ClimateSoil
Animal
Coccidioides
ClimateSoil
Animal
Coccidioides
Animals have to eat.
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ClimateSoil
Plant Animal
Coccidioides
ClimateSoil
Plant Animal
Coccidioides
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ClimateSoil
Plant Animal
Coccidioides
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Maricopa
Avenal
California State Hwy 33
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California State Hwy 33
The CocciDx assay*Coccidioides-Specific PCR Assay
Targeting a Transposable Element
*CocciENV Assay. Bowers et al. 2018 Med Mycol doi: 10.1093/mmy/myy007
10/2/2018
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Maricopa
Avenal
Coccidioides detectedin burrows at all sites
Maricopa
Avenal
Coccidioides detectedat surface at two sites
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Maricopa
Avenal
Sites where road workers have
contracted coccidioidomycosis.
Maricopa
Avenal
Sites where road workers have
contracted coccidioidomycosis.
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LivingMammal
DeadMammal
Life cycle
Arthroconidia
Taylor and Barker 2018 Med Mycol
LivingMammal
DeadMammal
Long distance dispersal in air
Short distance dispersal in
soil
Life cycle
Arthroconidia
Taylor and Barker 2018 Med Mycol
10/2/2018
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LivingMammal
DeadMammal
Long distance dispersal in air
Short distance dispersal in
soilMammal inhales
arthroconidia
Life cycle
Taylor and Barker 2018 Med Mycol
LivingMammal
DeadMammal
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Taylor and Barker 2018 Med Mycol
10/2/2018
40
LivingMammal
DeadMammal
Dissemination via fungal endospores.
Short host life
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Spherules develop
Taylor and Barker 2018 Med Mycol
LivingMammal
DeadMammal
Containment inhost granuloma.
Long host life.
Dissemination via fungal endospores.
Short host life
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Spherules develop
Taylor and Barker 2018 Med Mycol
10/2/2018
41
LivingMammal
DeadMammal
Containment inhost granuloma.
Long host life.
Dissemination via fungal endospores.
Short host life
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Spherules develop
Taylor and Barker 2018 Med Mycol
LivingMammal
DeadMammal
Containment inhost granuloma.
Long host life.
Dissemination via fungal endospores.
Short host life
Hyphae grow in dead host and produce
arthroconidia
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Arthroconidia
Taylor and Barker 2018 Med Mycol
Spherules develop
10/2/2018
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LivingMammal
DeadMammal
Containment inhost granuloma.
Long host life.
Dissemination via fungal endospores.
Short host life
Hyphae grow in dead host and produce
arthroconidia
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Arthroconidia
Taylor and Barker 2018 Med Mycol
Spherules develop
Taylor and Barker 2018 Med Mycol
Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
10/2/2018
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Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
What do other data say?
Solar Panel Farms
Carrizo Plain: Drought, Plants and Mammals
Cocci in agriculture
Carrizo Plain National Monument
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10/2/2018
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MMWR / August 24, 2018 / Vol. 67 / No. 33
MMWR / August 24, 2018 / Vol. 67 / No. 33
Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.
The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.
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MMWR / August 24, 2018 / Vol. 67 / No. 33
Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.
The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.
LivingMammal
DeadMammal
Containment inhost granuloma.
Long host life.
Dissemination via fungal endospores.
Short host life
Hyphae grow in dead host and produce
arthroconidia
Long distance dispersal in air
Short distance dispersal in
soil
Spherules develop
Mammal inhales arthroconidia
Life cycle
Arthroconidia
Spherules develop
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Nature Climate Change 8:819-824 (2018)
Here [Carrizo Plain], we quantified the responses of 423 sympatric
species of plants, arthropods, birds, reptiles and mammals to California’s
drought of 2012–2015—the driest period in the past 1,200 years for this
global biodiversity hotspot.
Nature Climate Change 8, pages819–824 (2018)
Nature Climate Change 8:819-824 (2018)
Here [Carrizo Plain], we quantified the responses of 423 sympatric
species of plants, arthropods, birds, reptiles and mammals to California’s
drought of 2012–2015—the driest period in the past 1,200 years for this
global biodiversity hotspot.
Nature Climate Change 8, pages819–824 (2018)
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Mammals (n=15)
Plants (n=61)
Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05
Losers Winners
Mammals (n=15)
Plants (n=61)
Losers Winners
Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05
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Prugh et al. 2018 Nature Climate Change
Drought Index
Plants
Prugh et al. 2018 Nature Climate Change
Drought Index Drought Index
Plants Rodents
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Prugh et al. 2018 Nature Climate ChangeOne rodent, the Giant Kangaroo Rat, was very abundant (86%) pre-drought
Plants Rodents
https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf
Millim
eters of P
recipitatio
n
Rain Human Cocci
Prugh et al. 2018 Nature Climate Change
10/2/2018
52
ClimateSoil
Plant Animal
Coccidioides
ClimateSoil
Plant Animal
Coccidioides
Is Coccidioides absent from cultivated land?
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53
ClimateSoil
Plant Animal
Coccidioides
Is Coccidioides absent from cultivated land?
ClimateSoil
Plant Animal
Coccidioides
Is Coccidioides absent from cultivated land?
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Arizona Medicine 1965 22: 281-288
1965
Even in areas highly infective for man, fungus was only isolated in non-cultivated and non-irrigated soils.
Kevin T. Maddy, DVM, MPH
Is Coccidioides absent from cultivated land?
Maricopa
Avenal
Coccidioides detectedin burrows at all sites
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6 Sites
72 soil samples
8.7M ITS1 reads
Native Soils
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1 site, 6 plots
102 Soil Samples
8.8M ITS1 reads
Agricultural Soils
Native, 3,600 OTUs Agricultural. 900 OTUs
Ascos
Fungi
Basidios
Zygos
Chytrids
Ascos
FungiBasidios
Zygos
ChytridsPhyla of Fungi
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Native, 1492 OTUs
Classes of Ascomycota
Agricultural 495 OTUs
Dothideomycetes
Sordariomycetes
Eurotiomycetes
Leotiomycetes
Lecanoromycetes
Pezizomycetes
Ascomycota
Dothideomycetes
Sordariomycetes
Eurotiomycetes
Leotiomycetes
Pezizomycetes
AscomycotaSaccharomycetes
Orders of Eurotiomycetes
Native Soils, 244 OTUs Agricultural Soils, 70 OTUs
Eurotiales
Chaetothyriales
Onygenales
Eurotiomycetes
Eurotiales
Chaetothyriales
Onygenales
Eurotiomycetes
21 OTUS
70 OTUS
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OTU Genus (Taxon) % Reads
Chrysosporium 21.2%
Gymnoascaceae 19.0%
Chrysosporium 17.3%
Spiromastix 16.1%
Auxarthron 2.5%
Coccidioides 2.2%
Chrysosporium 2.0%
Spiromastix 2.0%
Onygenales 2.0%
Auxarthron 1.8%
Auxarthron 1.2%
Native, 70 OTUs Agricultural, 21 OTUs
Onygenales most common OTUs
OTU Genus % Reads
Gymnoascus 31.7%
Chrysosporium 19.9%
Chrysosporium 9.7%
Chrysosporium 9.2%
Spiromastix 6.5%
Uncinocarpus 5.9%
Chrysosporium 4.7%
Chrysosporium 3.9%
Myceliophthora 3.6%
Onygenales 2.7%
Gymnoascoideus 1.0%
OTU Genus (Taxon) % Reads
Chrysosporium 21.2%
Gymnoascaceae 19.0%
Chrysosporium 17.3%
Spiromastix 16.1%
Auxarthron 2.5%
Coccidioides 2.2%
Chrysosporium 2.0%
Spiromastix 2.0%
Onygenales 2.0%
Auxarthron 1.8%
Auxarthron 1.2%
OTU Genus % Reads
Gymnoascus 31.7%
Chrysosporium 19.9%
Chrysosporium 9.7%
Chrysosporium 9.2%
Spiromastix 6.5%
Uncinocarpus 5.9%
Chrysosporium 4.7%
Chrysosporium 3.9%
Myceliophthora 3.6%
Onygenales 2.7%
Gymnoascoideus 1.0%
Onygenales most common OTUs
Native, 70 OTUs Agricultural, 21 OTUs
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OTU Genus (Taxon) % Reads
Chrysosporium 21.2%
Gymnoascaceae 19.0%
Chrysosporium 17.3%
Spiromastix 16.1%
Auxarthron 2.5%
Coccidioides 2.2%
Chrysosporium 2.0%
Spiromastix 2.0%
Onygenales 2.0%
Auxarthron 1.8%
Auxarthron 1.2%
OTU Genus % Reads
Gymnoascus 31.7%
Chrysosporium 19.9%
Chrysosporium 9.7%
Chrysosporium 9.2%
Spiromastix 6.5%
Uncinocarpus 5.9%
Chrysosporium 4.7%
Chrysosporium 3.9%
Myceliophthora 3.6%
Onygenales 2.7%
Gymnoascoideus 1.0%
Onygenales most common OTUs
Native, 70 OTUs Agricultural, 21 OTUs
ClimateSoil
Plant Animal
Coccidioides
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ClimateSoil
Plant Animal
Coccidioides
ClimateSoil
Plant Animal
Coccidioides
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• Peggy Lemaux
• Cheng Gao
• Liliam Montoya
• Devin Coleman-Derr
• Jeff Dahlberg
• Anita Sil
• Rachel Brem
• Clarissa Nobile
• Katrina Hoyer
• Aaron Hernday
• Josh Fierer
• Jason Stajich
• Bridget Barker
• Vishnu Chaturvedi
• Jessie Uehling
10/2/2018
62
• Peggy Lemaux
• Cheng Gao
• Liliam Montoya
• Devin Coleman-Derr
• Jeff Dahlberg
• Anita Sil
• Rachel Brem
• Clarissa Nobile
• Katrina Hoyer
• Aaron Hernday
• Josh Fierer
• Jason Stajich
• Bridget Barker
• Vishnu Chaturvedi
• Jessie Uehling
Questions?
10/2/2018
63
?
Cocci found in Native American middens
Cocci absent from surrounding soil and rodents
10/2/2018
64
?
A midden is an old dump for domestic waste which may consist of animal bone, human excrement, botanical material, and remnants of food, pottery, tools and other artifacts and
ecofacts associated with past human occupation.
?https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.
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65
?https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.
?https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern FUNGAL communities.
10/2/2018
66
?https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern FUNGAL communities.
Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.
?
Cocci found in Native American middens
Cocci absent from surrounding soil and rodents
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67
Coccidioides Texeira et al. 2016 doi 10.3201/eid2206.151565Engelthaller et al. 2016 doi 10.1128/mBio.00550-
16Histoplasma Sepúlveda et al. 2017. doi 10.1128/mBio.01339-17Blastomyces Jiang et al. 2018. doi 10.1007/s13225-018-0403-yParacoccidioides Muñoz et al, 2016. doi 10.1128/mSphere.00213-16 Emergomyces Schwartz et al. 2018. doi 10.1007/s12281-018-0308-y
CoccidioidesHistoplasmaBlastomyces
ParacoccidioidesEmergomyces
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Prugh et al. 2018 Nature Climate Change
Plants
MammalsArthropods
Birds
Response to one year of drought
Winners
Losers
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Millim
eters of P
recipitatio
n