Nitrous oxide producing activity of diverse fungi from distinct agroecosystems

Mothapo, Nape V.; Chen, Huaihai; Cubeta, Marc A.; Shi, Wei

doi:10.1016/j.soilbio.2013.07.004

Cited by 61 publications

(44 citation statements)

References 43 publications

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“…Studies have suggested that denitrification is a widespread trait of cultivable soil-inhabiting fungi and that fungal denitrifiers can be found in various soil ecosystems (17,42). Based on the available literature and the results obtained in this study, Fusarium species are the most often reported fungal denitrifiers (13), suggesting that this genus plays a significant role in N 2 O production from soil.…”

Section: Discussionsupporting

confidence: 54%

“…Based on the available literature and the results obtained in this study, Fusarium species are the most often reported fungal denitrifiers (13), suggesting that this genus plays a significant role in N 2 O production from soil. The diversity and the identity of soil-inhabiting fungi that are capable of denitrification is not well known, as many studies are finding new species of denitrifying fungi (16,17,42).…”

Section: Discussionmentioning

confidence: 99%

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Novel P450nor Gene Detection Assay Used To Characterize the Prevalence and Diversity of Soil Fungal Denitrifiers

Novinscak

Zebarth

Burton

et al. 2016

Appl Environ Microbiol

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Denitrifying fungi produce nitrous oxide (N 2 O), a potent greenhouse gas, as they generally lack the ability to convert N 2 O to dinitrogen. Contrary to the case for bacterial denitrifiers, the prevalence and diversity of denitrifying fungi found in the environment are not well characterized. In this study, denitrifying fungi were isolated from various soil ecosystems, and novel PCR primers targeting the P450nor gene, encoding the enzyme responsible for the conversion of nitric oxide to N 2 O, were developed, validated, and used to study the diversity of cultivable fungal denitrifiers. This PCR assay was also used to detect P450nor genes directly from environmental soil samples. Fungal denitrification capabilities were further validated using an N 2 O gas detection assay and a PCR assay targeting the nirK gene. A collection of 492 facultative anaerobic fungi was isolated from 15 soil ecosystems and taxonomically identified by sequencing the internal transcribed spacer sequence. Twenty-seven fungal denitrifiers belonging to 10 genera had the P450nor and the nirK genes and produced N 2 O from nitrite. N 2 O production is reported in strains not commonly known as denitrifiers, such as Byssochlamys nivea, Volutella ciliata, Chloridium spp., and Trichocladium spp. The prevalence of fungal denitrifiers did not follow a soil ecosystem distribution; however, a higher diversity was observed in compost and agricultural soils. The phylogenetic trees constructed using partial P450nor and nirK gene sequences revealed that both genes clustered taxonomically closely related strains together. IMPORTANCE A PCR assay targeting the P450nor gene involved in fungal denitrification was developed and validated. The newly developedP450nor primers were used on fungal DNA extracted from a collection of fungi isolated from various soil environments and on DNA directly extracted from soil. The results indicated that approximatively 25% of all isolated fungi possessed this gene and were able to convert nitrite to N 2 O. All soil samples from which denitrifying fungi were isolated also tested positive for the presence of P450nor. The P450nor gene detection assay was reliable in detecting a large diversity of fungal denitrifiers. Due to the lack of homology existing between P450nor and bacterial denitrification genes, it is expected that this assay will become a tool of choice for studying fungal denitrifiers.

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Section: Discussionsupporting

confidence: 54%

Section: Discussionmentioning

confidence: 99%

Novel P450nor Gene Detection Assay Used To Characterize the Prevalence and Diversity of Soil Fungal Denitrifiers

Novinscak

Zebarth

Burton

et al. 2016

Appl Environ Microbiol

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“…For example, several members of the genera Fusarium and Trichoderma, both known to harbor species capable of N 2 O production, were cultured (8,17,18). Also identified were two Mortierella isolates (Mortierellomycotina, formally Zygomycota), a genus that includes members known to produce N 2 O (33, 58).…”

Section: Figmentioning

confidence: 99%

“…Potential roles of fungi in soil N loss and greenhouse gas (i.e., N 2 O) emission are underexplored, and monitoring tools (e.g., quantitative or endpoint PCR) to specifically address the presence and abundance of denitrifying fungi are largely lacking. To date, the majority of the known denitrifying fungal isolates reside in the phylum Ascomycota (7)(8)(9). Although some reports suggest that fungi within the Basidiomycota and Zygomycota are denitrifiers (8)(9)(10), only a few isolates are available, and it remains to be confirmed if members of other phyla harbor nar, nap, nir, and nor gene clusters implicated in steps of the denitrification pathway.…”

mentioning

confidence: 99%

“…To date, the majority of the known denitrifying fungal isolates reside in the phylum Ascomycota (7)(8)(9). Although some reports suggest that fungi within the Basidiomycota and Zygomycota are denitrifiers (8)(9)(10), only a few isolates are available, and it remains to be confirmed if members of other phyla harbor nar, nap, nir, and nor gene clusters implicated in steps of the denitrification pathway. Previous investigations of fungal denitrification have relied on laboratory cultivation and substrate-induced respiration inhibition (SIRIN) tests (3,7,10).…”

mentioning

confidence: 99%

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Detection and Diversity of Fungal Nitric Oxide Reductase Genes ( p450nor ) in Agricultural Soils

Higgins

Welsh

Orellana

et al. 2016

Appl Environ Microbiol

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Members of the Fungi convert nitrate (NO 3؊ ) and nitrite (NO 2 ؊ ) to gaseous nitrous oxide (N 2 O) (denitrification), but the fungal contributions to N loss from soil remain uncertain. Cultivation-based methodologies that include antibiotics to selectively assess fungal activities have limitations, and complementary molecular approaches to assign denitrification potential to fungi are desirable. Microcosms established with soils from two representative U.S. Midwest agricultural regions produced N 2 O from added NO 3 ؊ or NO 2 ؊ in the presence of antibiotics to inhibit bacteria. Cultivation efforts yielded 214 fungal isolates belonging to at least 15 distinct morphological groups, 151 of which produced N 2 O from NO 2 ؊ . Novel PCR primers targeting the p450nor gene, which encodes the nitric oxide (NO) reductase responsible for N 2 O production in fungi, yielded 26 novel p450nor amplicons from DNA of 37 isolates and 23 amplicons from environmental DNA obtained from two agricultural soils. The sequences shared 54 to 98% amino acid identity with reference P450nor sequences within the phylum Ascomycota and expand the known fungal P450nor sequence diversity. p450nor was detected in all fungal isolates that produced N 2 O from NO 2 ؊ , whereas nirK (encoding the NO-forming NO 2 ؊ reductase) was amplified in only 13 to 74% of the N 2 O-forming isolates using two separate nirK primer sets. Collectively, our findings demonstrate the value of p450nor-targeted PCR to complement existing approaches to assess the fungal contributions to denitrification and N 2 O formation. IMPORTANCEA comprehensive understanding of the microbiota controlling soil N loss and greenhouse gas (N 2 O) emissions is crucial for sustainable agricultural practices and addressing climate change concerns. We report the design and application of a novel PCR primer set targeting fungal p450nor, a biomarker for fungal N 2 O production, and demonstrate the utility of the new approach to assess fungal denitrification potential in fungal isolates and agricultural soils. These new PCR primers may find application in a variety of biomes to assess the fungal contributions to N loss and N 2 O emissions. Denitrification is a key process responsible for loss of fixed nitrogen (N) in soils and sediments and is mediated by both abiotic and microbial processes (1, 2). Of the microorganisms involved in denitrification, members of the Bacteria are well studied and considered key contributors; however, some saprotrophic fungi also conserve energy from the reduction of nitrate (NO 3 Ϫ ) or nitrite (NO 2 Ϫ ) to nitrous oxide (N 2 O), the main end product of fungal denitrification (3-5). Fungi have been implicated in N turnover for over 30 years (1,3,6), but the ecological importance of fungal contributions to denitrification remain uncertain. Potential roles of fungi in soil N loss and greenhouse gas (i.e., N 2 O) emission are underexplored, and monitoring tools (e.g., quantitative or endpoint PCR) to specifically address the presence and abundance of denitrif...

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2019

The Science of Climate Change

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Nitrous oxide producing activity of diverse fungi from distinct agroecosystems

Cited by 61 publications

References 43 publications

Novel P450nor Gene Detection Assay Used To Characterize the Prevalence and Diversity of Soil Fungal Denitrifiers

Novel P450nor Gene Detection Assay Used To Characterize the Prevalence and Diversity of Soil Fungal Denitrifiers

Detection and Diversity of Fungal Nitric Oxide Reductase Genes ( p450nor ) in Agricultural Soils

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