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      Strong sesquiterpene emissions from Amazonian soils

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          Abstract

          The Amazon rainforest is the world’s largest source of reactive volatile isoprenoids to the atmosphere. It is generally assumed that these emissions are products of photosynthetically driven secondary metabolism and released from the rainforest canopy from where they influence the oxidative capacity of the atmosphere. However, recent measurements indicate that further sources of volatiles are present. Here we show that soil microorganisms are a strong, unaccounted source of highly reactive and previously unreported sesquiterpenes (C 15H 24; SQT). The emission rate and chemical speciation of soil SQTs were determined as a function of soil moisture, oxygen, and rRNA transcript abundance in the laboratory. Based on these results, a model was developed to predict soil–atmosphere SQT fluxes. It was found SQT emissions from a Terra Firme soil in the dry season were in comparable magnitude to current global model canopy emissions, establishing an important ecological connection between soil microbes and atmospherically relevant SQTs.

          Abstract

          Recent measurements in the Amazon rainforest indicate missing sources of volatile organic compounds (VOCs). Here the authors show that soil microorganisms are a strong, unaccounted source of highly reactive sesquiterpenes, a class of VOCs that can regulate ozone chemistry within the forest canopy.

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          Recruitment of entomopathogenic nematodes by insect-damaged maize roots.

          Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E)-beta-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E)-beta-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-beta-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.
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            Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses.

            Microbes exist in a range of metabolic states (for example, dormant, active and growing) and analysis of ribosomal RNA (rRNA) is frequently employed to identify the 'active' fraction of microbes in environmental samples. While rRNA analyses are no longer commonly used to quantify a population's growth rate in mixed communities, due to rRNA concentration not scaling linearly with growth rate uniformly across taxa, rRNA analyses are still frequently used toward the more conservative goal of identifying populations that are currently active in a mixed community. Yet, evidence indicates that the general use of rRNA as a reliable indicator of metabolic state in microbial assemblages has serious limitations. This report highlights the complex and often contradictory relationships between rRNA, growth and activity. Potential mechanisms for confounding rRNA patterns are discussed, including differences in life histories, life strategies and non-growth activities. Ways in which rRNA data can be used for useful characterization of microbial assemblages are presented, along with questions to be addressed in future studies.
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              Responses of soil bacterial and fungal communities to extreme desiccation and rewetting.

              The microbial response to summer desiccation reflects adaptation strategies, setting the stage for a large rainfall-induced soil CO2 pulse upon rewetting, an important component of the ecosystem carbon budget. In three California annual grasslands, the present (DNA-based) and potentially active (RNA-based) soil bacterial and fungal communities were tracked over a summer season and in response to controlled rewetting of intact soil cores. Phylogenetic marker genes for bacterial (16S) and fungal (28S) RNA and DNA were sequenced, and the abundances of these genes and transcripts were measured. Although bacterial community composition differed among sites, all sites shared a similar response pattern of the present and potentially active bacterial community to dry-down and wet-up. In contrast, the fungal community was not detectably different among sites, and was largely unaffected by dry-down, showing marked resistance to dessication. The potentially active bacterial community changed significantly as summer dry-down progressed, then returned to pre-dry-down composition within several hours of rewetting, displaying spectacular resilience. Upon rewetting, transcript copies of bacterial rpoB genes increased consistently, reflecting rapid activity resumption. Acidobacteria and Actinobacteria were the most abundant phyla present and potentially active, and showed the largest changes in relative abundance. The relative increase (Actinobacteria) and decrease (Acidobacteria) with dry-down, and the reverse responses to rewetting reflected a differential response, which was conserved at the phylum level and consistent across sites. These contrasting desiccation-related bacterial life-strategies suggest that predicted changes in precipitation patterns may affect soil nutrient and carbon cycling by differentially impacting activity patterns of microbial communities.
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                Author and article information

                Contributors
                e.bourtsoukidis@mpic.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                8 June 2018
                8 June 2018
                2018
                : 9
                : 2226
                Affiliations
                [1 ]ISNI 0000 0004 0491 8257, GRID grid.419509.0, Atmospheric Chemistry and Biogeochemistry Departments, , Max Planck Institute for Chemistry, ; Hahn-Meitner-Weg 1, 55128 Mainz, Germany
                [2 ]ISNI 0000 0004 0491 7318, GRID grid.419500.9, Max Planck Institute for Biogeochemistry, ; Hans-Knöll-Straße 10, 07745 Jena, Germany
                [3 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, National Institute of Amazonian Research, ; Av. André Araújo, 2936 - Petrópolis, Manaus, AM 69067-375 Brazil
                [4 ]ISNI 0000 0001 2253 8678, GRID grid.8657.c, Finnish Meteorological Institute, ; Erik Palménin aukio 1, FI-00560 Helsinki, Finland
                [5 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Department of Plant and Environmental Science, , University of Copenhagen, ; Thorvaldsensvej 40, 1871 Frederiksberg C, DK-1871 Copenhagen, Denmark
                [6 ]ISNI 0000 0000 8190 6402, GRID grid.9835.7, Lancaster Environment Centre, , Lancaster University, ; Lancaster, LA1 4YQ UK
                [7 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, University of Sao Paulo, ; Rua do Matão, Travessa R, 187, São Paulo, SP CEP 05508-900 Brazil
                [8 ]GRID grid.5963.9, Present Address: University of Freiburg, ; Georges-Köhler-Allee 53, 79110 Freiburg, Germany
                [9 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Present Address: Imperial College London, ; London, SW7 2AZ UK
                [10 ]ISNI 0000000115480420, GRID grid.7907.9, Present Address: Laboratory of Atmospheric Physics (LaMP), , University Blaise Pascal, ; 63000 Clermont-Ferrand, France
                Author information
                http://orcid.org/0000-0001-5578-9414
                http://orcid.org/0000-0001-6408-5961
                http://orcid.org/0000-0003-2440-6104
                http://orcid.org/0000-0002-4420-9442
                http://orcid.org/0000-0002-4446-534X
                http://orcid.org/0000-0001-6307-3846
                Article
                4658
                10.1038/s41467-018-04658-y
                5993744
                29884892
                6354d171-32b8-40d8-83d7-c57d84f1cbd8
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 4 September 2017
                : 15 May 2018
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