Expanding the environmental virome: Infection profile in a native rainforest tree species

Anderson Carvalho Vieira; Ícaro Santos Lopes; Paula Luize Camargos Fonseca; Roenick Proveti Olmo; Flora Bittencourt; Letícia Maróstica de Vasconcelos; Carlos Priminho Pirovani; Fernanda Amato Gaiotto; Eric Roberto Guimarães Rocha Aguiar

doi:10.3389/fmicb.2022.874319

Expanding the environmental virome: Infection profile in a native rainforest tree species

Front Microbiol. 2022 Aug 4:13:874319. doi: 10.3389/fmicb.2022.874319. eCollection 2022.

Authors

Anderson Carvalho Vieira¹, Ícaro Santos Lopes², Paula Luize Camargos Fonseca^{1

3}, Roenick Proveti Olmo⁴, Flora Bittencourt¹, Letícia Maróstica de Vasconcelos¹, Carlos Priminho Pirovani¹, Fernanda Amato Gaiotto¹, Eric Roberto Guimarães Rocha Aguiar¹

Affiliations

¹ Department of Biological Science, Center of Biotechnology and Genetics, Universidade Estadual de Santa Cruz, Ilhéus, Brazil.
² Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
³ Department of Genetics, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
⁴ Université de Strasbourg, CNRS UPR9022, Inserm, Strasbourg, France.

Abstract

Agroforestry systems (AFS) for cocoa production combine traditional land-use practices with local biodiversity conservation, resulting in both ecological and agricultural benefits. The cacao-cabruca AFS model is widely implemented in regions of the Brazilian Atlantic Forest. Carpotroche brasiliensis (Raddi) A. Gray (Achariaceae) is a tree found in cabruca landscapes that is often used for reforestation and biotechnological applications. Despite its importance, we still lack information about viruses circulating in C. brasiliensis, particularly considering the possibility of spillover that could affect cocoa production. In our study, we analyzed the Carpotroche brasiliensis virome from Atlantic Forest and cacao-cabruca AFS regions using metatranscriptomics from several vegetative and reproductive organs. Our results revealed a diverse virome detecting near-complete or partial coding sequences of single- and double-stranded DNA and RNA viruses classified into at least six families (Botourmiaviridae, Bromoviridae, Caulimoviridae, Genomoviridae, Mitoviridae, and Rhabdoviridae) plus unclassified elements. We described with high confidence the near-complete and the partial genomes of two tentative novel viruses: Carpotroche-associated ilarvirus and Carpotroche-associated genomovirus, respectively. Interestingly, we also described sequences likely derived from a rhabdovirus, which could represent a novel member of the genus Gammanucleorhabdovirus. We observed higher viral diversity in cacao-cabruca AFS and reproductive organs of C. brasiliensis with preferential tropism to fruits, which could directly affect production. Altogether, our results provide data to better understand the virome in this unexplored agroecological interface, such as cacao-cabruca AFS and forest ecosystem, providing information on the aspects of virus-plant interactions.

Keywords: Carpotroche brasiliensis; agroforestry; metatranscriptomics; rainforest tree; virome.