Presence and distribution of insect-associated and entomopathogenic fungi in a temperate pine forest soil: An integrated approach

Deaver, Noland R.; Hesse, Cedar; Kuske, Cheryl Rae; Porras-Alfaro, Andrea

doi:10.1016/j.funbio.2019.09.006

Title: Presence and distribution of insect-associated and entomopathogenic fungi in a temperate pine forest soil: An integrated approach

Journal Article · 23 September 2019 · Fungal Biology

DOI: https://doi.org/10.1016/j.funbio.2019.09.006 · OSTI ID:1569616

Deaver, Noland R. ^[1]; Hesse, Cedar ^[2];

^[3];

^[1]

Western Illinois Univ., Macomb, IL (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States); United States Department of Agriculture, Corvallis, OR (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

For decades entomopathogenic fungi have garnered interest as possible alternatives to chemical pesticides. However, their ecology outside of agroecosystems demands further study. We assessed the diversity and abundance of entomopathogenic and insect-associated fungi at a loblolly pine forest in North Carolina, USA using culture-dependent and next-generation sequencing libraries. Fungi were isolated using Galleria mellonella larvae, as well as from soil dilutions plated on a selective medium. Isolates were identified using Sanger sequencing of the ITS and LSU rRNA gene regions, and represented 36 OTUs including Metarhizium, Lecanicillium, and Paecilomyces. Additionally, we assessed the chitinolytic potential of isolates and found widespread, variable ability to degrade chitin within and between genera. Phylogenetic analyses resolved several isolates to genus, with some forming clades with other insect-associated taxa, as well as with fungi associated with plant tissues. Saprophytes were widely distributed in soil, while entomopathogens were less abundant and present primarily in the top two cm of the soil. Furthermore, the similarity between culture-dependent and next-generation sequencing results demonstrates that both methods can be used concurrently in this system to study the ecology of entomopathogenic fungi.

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Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1569616

Report Number(s):: LA-UR--19-20465

Journal Information:: Fungal Biology, Journal Name: Fungal Biology Journal Issue: 12 Vol. 123; ISSN 1878-6146

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

Entomopathogenic Isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus Produce Multiple Extracellular Chitinase Isozymes St. Leger, Raymond J.; Staples, Richard C.; Roberts, Donald W. Journal of Invertebrate Pathology, Vol. 61, Issue 1 https://doi.org/10.1006/jipa.1993.1014	journal	January 1993
Carbon source control on β-glucanases, chitobiase and chitinase from Trichoderma harzianum de la Cruz, Jesús; Rey, Manuel; Lora, José M. Archives of Microbiology, Vol. 159, Issue 4 https://doi.org/10.1007/BF00290913	journal	April 1993
Genetic groups of the insect-pathogenic fungus Beauveria bassiana are associated with habitat and thermal growth preferences Bidochka, Michael; Menzies, Fiona; Kamp, Andrena Archives of Microbiology, Vol. 178, Issue 6 https://doi.org/10.1007/s00203-002-0490-7	journal	December 2002
Distribution of Chitinases in the Entomopathogen Metarhizium anisopliae and Effect of N -Acetylglucosamine in Protein Secretion Barreto, Cristine Chaves; Staats, Charley Christian; Schrank, Augusto Current Microbiology, Vol. 48, Issue 2 https://doi.org/10.1007/s00284-003-4063-z	journal	February 2004
The effects of farming system, habitat type and bait type on the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Province, South Africa Goble, T. A.; Dames, J. F.; P. Hill, M. BioControl, Vol. 55, Issue 3 https://doi.org/10.1007/s10526-009-9259-0	journal	December 2009
Review of Fungal Chitinases Duo-Chuan, Li Mycopathologia, Vol. 161, Issue 6 https://doi.org/10.1007/s11046-006-0024-y	journal	June 2006
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Spatial distribution of fungal and bacterial biomass in southern Ohio hardwood forest soils: fine scale variability and microscale patterns Morris, S. Soil Biology and Biochemistry, Vol. 31, Issue 10 https://doi.org/10.1016/S0038-0717(99)00047-4	journal	September 1999
Chitinolytic enzymes: an exploration Patil, Reetarani S.; Ghormade, Vandana; Deshpande, Mukund V. Enzyme and Microbial Technology, Vol. 26, Issue 7 https://doi.org/10.1016/S0141-0229(00)00134-4	journal	April 2000
Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils Klingen, Ingeborg; Eilenberg, Jørgen; Meadow, Richard Agriculture, Ecosystems & Environment, Vol. 91, Issue 1-3 https://doi.org/10.1016/S0167-8809(01)00227-4	journal	September 2002
Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils Chandler, D.; Hay, D.; Reid, A. P. Applied Soil Ecology, Vol. 5, Issue 2 https://doi.org/10.1016/S0929-1393(96)00144-8	journal	May 1997
Distribution and occurrence of four entomopathogenic fungi in Finland: effect of geographical location, habitat type and soil type Vänninen, Irene Mycological Research, Vol. 100, Issue 1 https://doi.org/10.1016/S0953-7562(96)80106-7	journal	January 1996
Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem Meyling, Nicolai V.; Eilenberg, Jørgen Agriculture, Ecosystems & Environment, Vol. 113, Issue 1-4 https://doi.org/10.1016/j.agee.2005.10.011	journal	April 2006
Occurrence and diversity of insect-associated fungi in natural soils in China Sun, Bing-Da; Liu, Xing-Zhong Applied Soil Ecology, Vol. 39, Issue 1 https://doi.org/10.1016/j.apsoil.2007.12.001	journal	May 2008
Presence and distribution of heavy metal tolerant fungi in surface soils of a temperate pine forest Torres-Cruz, Terry J.; Hesse, Cedar; Kuske, Cheryl R. Applied Soil Ecology, Vol. 131 https://doi.org/10.1016/j.apsoil.2018.08.001	journal	October 2018
Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils Uzman, Deniz; Pliester, Jasmin; Leyer, Ilona Applied Soil Ecology, Vol. 133 https://doi.org/10.1016/j.apsoil.2018.09.004	journal	January 2019
Entomopathogenic fungal endophytes Vega, Fernando E.; Posada, Francisco; Catherine Aime, M. Biological Control, Vol. 46, Issue 1 https://doi.org/10.1016/j.biocontrol.2008.01.008	journal	July 2008
CTC medium: A novel dodine-free selective medium for isolating entomopathogenic fungi, especially Metarhizium acridum, from soil Fernandes, Éverton K. K.; Keyser, Chad A.; Rangel, Drauzio E. N. Biological Control, Vol. 54, Issue 3 https://doi.org/10.1016/j.biocontrol.2010.05.009	journal	September 2010
Insect-associated fungi in soils of field crops and orchards Sun, Bing-Da; Yu, Han-ying; Chen, Amanda J. Crop Protection, Vol. 27, Issue 11 https://doi.org/10.1016/j.cropro.2008.07.010	journal	November 2008
Fungal entomopathogens: new insights on their ecology Vega, Fernando E.; Goettel, Mark S.; Blackwell, Meredith Fungal Ecology, Vol. 2, Issue 4 https://doi.org/10.1016/j.funeco.2009.05.001	journal	November 2009
Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.) Akello, Juliet; Dubois, Thomas; Gold, Clifford S. Journal of Invertebrate Pathology, Vol. 96, Issue 1 https://doi.org/10.1016/j.jip.2007.02.004	journal	September 2007
Entomopathogenic fungi in cornfields and their potential to manage larval western corn rootworm Diabrotica virgifera virgifera Rudeen, Melissa L.; Jaronski, Stefan T.; Petzold-Maxwell, Jennifer L. Journal of Invertebrate Pathology, Vol. 114, Issue 3 https://doi.org/10.1016/j.jip.2013.09.009	journal	November 2013
Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils Quesada-Moraga, Enrique; Navas-Cortés, Juan A.; Maranhao, Elizabeth A. A. Mycological Research, Vol. 111, Issue 8 https://doi.org/10.1016/j.mycres.2007.06.006	journal	August 2007
Insecticide Resistance Signals Negative Consequences of Widespread Neonicotinoid Use on Multiple Field Crops in the U.S. Cotton Belt Huseth, Anders S.; Chappell, Thomas M.; Chitturi, Anitha Environmental Science & Technology, Vol. 52, Issue 4 https://doi.org/10.1021/acs.est.7b06015	journal	January 2018
Study on the communities of endophytic fungi and endophytic actinomycetes from rice and their antipathogenic activities in vitro Tian, X. L.; Cao, L. X.; Tan, H. M. World Journal of Microbiology and Biotechnology, Vol. 20, Issue 3 https://doi.org/10.1023/B:WIBI.0000023843.83692.3f	journal	January 2004
Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi Schoch, C. L.; Seifert, K. A.; Huhndorf, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1117018109	journal	March 2012
Evolutionary relationships among mucoralean fungi (Zygomycota): Evidence for family polyphyly on a large scale O'Donnell, Kerry; Lutzoni, François M.; Ward, Todd J. Mycologia, Vol. 93, Issue 2 https://doi.org/10.1080/00275514.2001.12063160	journal	March 2001
Phylogeny of the Zygomycota based on nuclear ribosomal sequence data White, Merlin M.; James, Timothy Y.; O’Donnell, Kerry Mycologia, Vol. 98, Issue 6 https://doi.org/10.1080/15572536.2006.11832617	journal	November 2006
An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny Zhang, Ning; Castlebury, Lisa A.; Miller, Andrew N. Mycologia, Vol. 98, Issue 6 https://doi.org/10.1080/15572536.2006.11832635	journal	November 2006
Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR Arnold, A. Elizabeth; Henk, Daniel A.; Eells, Rebecca L. Mycologia, Vol. 99, Issue 2 https://doi.org/10.1080/15572536.2007.11832578	journal	March 2007
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Chitinolytic Enzymes Produced by Trichoderma harzianum : Antifungal Activity of Purified Endochitinase and Chitobiosidase Lorito, M. Phytopathology, Vol. 83, Issue 3 https://doi.org/10.1094/Phyto-83-302	journal	January 1993
Plant and Bacterial Chitinases Differ in Antifungal Activity Roberts, W. K.; Selitrennikoff, C. P. Microbiology, Vol. 134, Issue 1 https://doi.org/10.1099/00221287-134-1-169	journal	January 1988
Community composition and population genetics of insect pathogenic fungi in the genus M etarhizium from soils of a long-term agricultural research system: Metarhizium Kepler, Ryan M.; Ugine, Todd A.; Maul, Jude E. Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12778	journal	March 2015
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences: SPECIES DELIMITATION IN FUNGAL ENDOPHYTES Gazis, Romina; Rehner, Stephen; Chaverri, Priscila Molecular Ecology, Vol. 20, Issue 14 https://doi.org/10.1111/j.1365-294X.2011.05110.x	journal	May 2011
Isolation and characterization of three chitinases from Trichoderma harzianum Cruz, Jesus; Hidalgo-Gallego, Antonio; Lora, Jose M. European Journal of Biochemistry, Vol. 206, Issue 3 https://doi.org/10.1111/j.1432-1033.1992.tb16994.x	journal	June 1992
Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development McCarthy, Heather R.; Oren, Ram; Johnsen, Kurt H. New Phytologist, Vol. 185, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03078.x	journal	November 2009
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Colonization of Corn, Zea mays, by the Entomopathogenic Fungus Beauveria bassiana Wagner, B. L.; Lewis, L. C. Applied and Environmental Microbiology, Vol. 66, Issue 8 https://doi.org/10.1128/AEM.66.8.3468-3473.2000	journal	August 2000
Habitat Association in Two Genetic Groups of the Insect-Pathogenic Fungus Metarhizium anisopliae: Uncovering Cryptic Species? Bidochka, Michael J.; Kamp, Andrena M.; Lavender, T. Michael Applied and Environmental Microbiology, Vol. 67, Issue 3 https://doi.org/10.1128/AEM.67.3.1335-1342.2001	journal	March 2001
Fungal Community Analysis by Large-Scale Sequencing of Environmental Samples O'Brien, H. E.; Parrent, J. L.; Jackson, J. A. Applied and Environmental Microbiology, Vol. 71, Issue 9 https://doi.org/10.1128/AEM.71.9.5544-5550.2005	journal	September 2005
Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Vilgalys, R.; Hester, M. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/JB.172.8.4238-4246.1990	journal	August 1990
Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs Rehner, Stephen A.; Samuels, Gary J. Canadian Journal of Botany, Vol. 73, Issue S1 https://doi.org/10.1139/b95-327	journal	December 1995
The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors Reid, Molly C.; McKenzie, F. Ellis Malaria Journal, Vol. 15, Issue 1 https://doi.org/10.1186/s12936-016-1162-4	journal	February 2016
Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits Lutzoni, François; Kauff, Frank; Cox, Cymon J. American Journal of Botany, Vol. 91, Issue 10 https://doi.org/10.3732/ajb.91.10.1446	journal	October 2004
A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA Wagner, L.; Stielow, B.; Hoffmann, K. Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 30, Issue 1 https://doi.org/10.3767/003158513X666268	journal	June 2013
Diversity and distribution of soil fungal communities in a semiarid grassland Porras-Alfaro, Andrea; Herrera, Jose; Natvig, Donald O. Mycologia, Vol. 103, Issue 1 https://doi.org/10.3852/09-297	journal	January 2011
Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana) Sharma, Lav; Oliveira, Irene; Torres, Laura MycoKeys, Vol. 38 https://doi.org/10.3897/mycokeys.38.26790	journal	August 2018

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59 BASIC BIOLOGICAL SCIENCES
Biological Science
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Next generation sequencing
Selective media
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Title: Presence and distribution of insect-associated and entomopathogenic fungi in a temperate pine forest soil: An integrated approach

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References (49)

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