Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities
Ammonia oxidation is the rate-limiting first step of nitrification and a key process in the nitrogen cycle that results in the formation of nitrite (NO2–), which can be further oxidized to nitrate (NO3–). In the Amazonian floodplains, soils are subjected to extended seasons of flooding during the ra...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-08-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.913453/full |
| _version_ | 1811222066823692288 |
|---|---|
| author | Gabriel G. T. N. Monteiro Dayane J. Barros Gabriele V. M. Gabriel Andressa M. Venturini Andressa M. Venturini Tomás G. R. Veloso Gisele H. Vazquez Luciana C. Oliveira Vania Neu Paul L. E. Bodelier Cleber Fernando M. Mansano Siu M. Tsai Acacio A. Navarrete Acacio A. Navarrete |
| author_facet | Gabriel G. T. N. Monteiro Dayane J. Barros Gabriele V. M. Gabriel Andressa M. Venturini Andressa M. Venturini Tomás G. R. Veloso Gisele H. Vazquez Luciana C. Oliveira Vania Neu Paul L. E. Bodelier Cleber Fernando M. Mansano Siu M. Tsai Acacio A. Navarrete Acacio A. Navarrete |
| author_sort | Gabriel G. T. N. Monteiro |
| collection | DOAJ |
| description | Ammonia oxidation is the rate-limiting first step of nitrification and a key process in the nitrogen cycle that results in the formation of nitrite (NO2–), which can be further oxidized to nitrate (NO3–). In the Amazonian floodplains, soils are subjected to extended seasons of flooding during the rainy season, in which they can become anoxic and produce a significant amount of methane (CH4). Various microorganisms in this anoxic environment can couple the reduction of different ions, such as NO2– and NO3–, with the oxidation of CH4 for energy production and effectively link the carbon and nitrogen cycle. Here, we addressed the composition of ammonium (NH4+) and NO3–—and NO2–—dependent CH4-oxidizing microbial communities in an Amazonian floodplain. In addition, we analyzed the influence of environmental and geochemical factors on these microbial communities. Soil samples were collected from different layers of forest and agroforest land-use systems during the flood and non-flood seasons in the floodplain of the Tocantins River, and next-generation sequencing of archaeal and bacterial 16S rRNA amplicons was performed, coupled with chemical characterization of the soils. We found that ammonia-oxidizing archaea (AOA) were more abundant than ammonia-oxidizing bacteria (AOB) during both flood and non-flood seasons. Nitrogen-dependent anaerobic methane oxidizers (N-DAMO) from both the archaeal and bacterial domains were also found in both seasons, with higher abundance in the flood season. The different seasons, land uses, and depths analyzed had a significant influence on the soil chemical factors and also affected the abundance and composition of AOA, AOB, and N-DAMO. During the flood season, there was a significant correlation between ammonia oxidizers and N-DAMO, indicating the possible role of these oxidizers in providing oxidized nitrogen species for methanotrophy under anaerobic conditions, which is essential for nitrogen removal in these soils. |
| first_indexed | 2024-04-12T08:10:19Z |
| format | Article |
| id | doaj.art-7ec71fb5086b4c5b9559d71d83f3c22e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-12T08:10:19Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-7ec71fb5086b4c5b9559d71d83f3c22e2022-12-22T03:41:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.913453913453Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communitiesGabriel G. T. N. Monteiro0Dayane J. Barros1Gabriele V. M. Gabriel2Andressa M. Venturini3Andressa M. Venturini4Tomás G. R. Veloso5Gisele H. Vazquez6Luciana C. Oliveira7Vania Neu8Paul L. E. Bodelier9Cleber Fernando M. Mansano10Siu M. Tsai11Acacio A. Navarrete12Acacio A. Navarrete13Federal Rural University of Amazonia (UFRA), Belém, BrazilGraduate Program in Biodiversity and Biotechnology (BIONORTE), Federal University of Tocantins (UFT), Palmas, BrazilGraduate Program in Biotechnology and Environmental Monitoring, Federal University of São Carlos (UFSCar), Sorocaba, BrazilCell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture, University of São Paulo (USP), Piracicaba, BrazilPrinceton Institute for International and Regional Studies, Princeton University, Princeton, NJ, United StatesGraduate Program in Agricultural Microbiology, Federal University of Viçosa, Viçosa, BrazilGraduate Program in Environmental Sciences, University Brazil, Fernandópolis, BrazilDepartment of Physics, Chemistry, and Mathematics, Federal University of São Carlos (UFSCar), Sorocaba, BrazilFederal Rural University of Amazonia (UFRA), Belém, BrazilDepartment of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsGraduate Program in Environmental Sciences, University Brazil, Fernandópolis, BrazilCell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture, University of São Paulo (USP), Piracicaba, BrazilCell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture, University of São Paulo (USP), Piracicaba, BrazilGraduate Program in Environmental Sciences, University Brazil, Fernandópolis, BrazilAmmonia oxidation is the rate-limiting first step of nitrification and a key process in the nitrogen cycle that results in the formation of nitrite (NO2–), which can be further oxidized to nitrate (NO3–). In the Amazonian floodplains, soils are subjected to extended seasons of flooding during the rainy season, in which they can become anoxic and produce a significant amount of methane (CH4). Various microorganisms in this anoxic environment can couple the reduction of different ions, such as NO2– and NO3–, with the oxidation of CH4 for energy production and effectively link the carbon and nitrogen cycle. Here, we addressed the composition of ammonium (NH4+) and NO3–—and NO2–—dependent CH4-oxidizing microbial communities in an Amazonian floodplain. In addition, we analyzed the influence of environmental and geochemical factors on these microbial communities. Soil samples were collected from different layers of forest and agroforest land-use systems during the flood and non-flood seasons in the floodplain of the Tocantins River, and next-generation sequencing of archaeal and bacterial 16S rRNA amplicons was performed, coupled with chemical characterization of the soils. We found that ammonia-oxidizing archaea (AOA) were more abundant than ammonia-oxidizing bacteria (AOB) during both flood and non-flood seasons. Nitrogen-dependent anaerobic methane oxidizers (N-DAMO) from both the archaeal and bacterial domains were also found in both seasons, with higher abundance in the flood season. The different seasons, land uses, and depths analyzed had a significant influence on the soil chemical factors and also affected the abundance and composition of AOA, AOB, and N-DAMO. During the flood season, there was a significant correlation between ammonia oxidizers and N-DAMO, indicating the possible role of these oxidizers in providing oxidized nitrogen species for methanotrophy under anaerobic conditions, which is essential for nitrogen removal in these soils.https://www.frontiersin.org/articles/10.3389/fmicb.2022.913453/fullammonia oxidationmethanotrophsThaumarchaeota16S rRNA sequencingtropical floodplains |
| spellingShingle | Gabriel G. T. N. Monteiro Dayane J. Barros Gabriele V. M. Gabriel Andressa M. Venturini Andressa M. Venturini Tomás G. R. Veloso Gisele H. Vazquez Luciana C. Oliveira Vania Neu Paul L. E. Bodelier Cleber Fernando M. Mansano Siu M. Tsai Acacio A. Navarrete Acacio A. Navarrete Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities Frontiers in Microbiology ammonia oxidation methanotrophs Thaumarchaeota 16S rRNA sequencing tropical floodplains |
| title | Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities |
| title_full | Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities |
| title_fullStr | Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities |
| title_full_unstemmed | Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities |
| title_short | Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities |
| title_sort | molecular evidence for stimulation of methane oxidation in amazonian floodplains by ammonia oxidizing communities |
| topic | ammonia oxidation methanotrophs Thaumarchaeota 16S rRNA sequencing tropical floodplains |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.913453/full |
| work_keys_str_mv | AT gabrielgtnmonteiro molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT dayanejbarros molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT gabrielevmgabriel molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT andressamventurini molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT andressamventurini molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT tomasgrveloso molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT giselehvazquez molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT lucianacoliveira molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT vanianeu molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT paullebodelier molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT cleberfernandommansano molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT siumtsai molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT acacioanavarrete molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities AT acacioanavarrete molecularevidenceforstimulationofmethaneoxidationinamazonianfloodplainsbyammoniaoxidizingcommunities |