Larvae of an invasive scarab increase greenhouse gas emissions from soils and recruit gut mycobiota involved in C and N transformations

Helena Avila-Arias; Ronald F Turco; Michael E Scharf; Russell L Groves; Douglas S Richmond

doi:10.3389/fmicb.2023.1102523

Larvae of an invasive scarab increase greenhouse gas emissions from soils and recruit gut mycobiota involved in C and N transformations

Front Microbiol. 2023 Mar 21:14:1102523. doi: 10.3389/fmicb.2023.1102523. eCollection 2023.

Authors

Helena Avila-Arias¹, Ronald F Turco², Michael E Scharf³, Russell L Groves⁴, Douglas S Richmond¹

Affiliations

¹ Department of Entomology, Purdue University, West Lafayette, IN, United States.
² Department of Agronomy, Purdue University, West Lafayette, IN, United States.
³ Entomology and Nematology Department, University of Florida, Gainesville, FL, United States.
⁴ Department of Entomology, University of Wisconsin-Madison, Madison, WI, United States.

Abstract

Background: Soil-derived prokaryotic gut communities of the Japanese beetle Popillia japonica Newman (JB) larval gut include heterotrophic, ammonia-oxidizing, and methanogenic microbes potentially capable of promoting greenhouse gas (GHG) emissions. However, no research has directly explored GHG emissions or the eukaryotic microbiota associated with the larval gut of this invasive species. In particular, fungi are frequently associated with the insect gut where they produce digestive enzymes and aid in nutrient acquisition. Using a series of laboratory and field experiments, this study aimed to (1) assess the impact of JB larvae on soil GHG emissions; (2) characterize gut mycobiota associated with these larvae; and (3) examine how soil biological and physicochemical characteristics influence variation in both GHG emissions and the composition of larval gut mycobiota.

Methods: Manipulative laboratory experiments consisted of microcosms containing increasing densities of JB larvae alone or in clean (uninfested) soil. Field experiments included 10 locations across Indiana and Wisconsin where gas samples from soils, as well as JB and their associated soil were collected to analyze soil GHG emissions, and mycobiota (ITS survey), respectively.

Results: In laboratory trials, emission rates of CO₂, CH₄, and N₂O from infested soil were ≥ 6.3× higher per larva than emissions from JB larvae alone whereas CO₂ emission rates from soils previously infested by JB larvae were 1.3× higher than emissions from JB larvae alone. In the field, JB larval density was a significant predictor of CO₂ emissions from infested soils, and both CO₂ and CH₄ emissions were higher in previously infested soils. We found that geographic location had the greatest influence on variation in larval gut mycobiota, although the effects of compartment (i.e., soil, midgut and hindgut) were also significant. There was substantial overlap in the composition and prevalence of the core fungal mycobiota across compartments with prominent fungal taxa being associated with cellulose degradation and prokaryotic methane production/consumption. Soil physicochemical characteristics such as organic matter, cation exchange capacity, sand, and water holding capacity, were also correlated with both soil GHG emission, and fungal a-diversity within the JB larval gut. Conclusions: Results indicate JB larvae promote GHG emissions from the soil directly through metabolic activities, and indirectly by creating soil conditions that favor GHG-associated microbial activity. Fungal communities associated with the JB larval gut are primarily influenced by adaptation to local soils, with many prominent members of that consortium potentially contributing to C and N transformations capable of influencing GHG emissions from infested soil.

Keywords: Japanese beetles; carbon dioxide; core mycobiota; fungal ITS1; methane; nitrous oxide.