Protist species richness and soil microbiome complexity increase towards climax vegetation in the Brazilian Cerrado

Abstract

Biodiversity underlies ecosystem functioning. While aboveground biodiversity is often well studied, the belowground microbiome, in particular protists, remains largely unknown. Indeed, holistic insights into soil microbiome structures in natural soils, especially in hyperdiverse biomes such as the Brazilian Cerrado, remain unexplored. Here, we study the soil microbiome across four major vegetation zones of the Cerrado, ranging from grass-dominated to tree-dominated vegetation with a focus on protists. We show that protist taxon richness increases towards the tree-dominated climax vegetation. Early successional habitats consisting of primary grass vegetation host most potential plant pathogens and least animal parasites. Using network analyses combining protist with prokaryotic and fungal sequences, we show that microbiome complexity increases towards climax vegetation. Together, this suggests that protists are key microbiome components and that vegetation succession towards climax vegetation is stimulated by higher loads of animal and plant pathogens. At the same time, an increase in microbiome complexity towards climax vegetation might enhance system stability.

Seasonal Variations in Soil Microbiota Profile of Termite (Syntermes wheeleri) Mounds in the Brazilian Tropical Savanna

“…The most abundant bacterial phyla found in the soil samples in this study were Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia, Chloroflexi, and Planctomycetes. These phyla are commonly found in soil samples as previously reported [ 12 , 16 , 24 , 34 , 35 , 36 ]. Most bacterial phyla in soil are rare; nonetheless, this “low abundance” part of the community represents 41% of total 16S rRNA gene sequences and are found in a great variety of soils [ 35 ].…”

Contrasting Responses of Protistan Plant Parasites and Phagotrophs to Ecosystems, Land Management and Soil Properties

“…One remarkable exception to the ubiquitous occurrence of our taxa was the endomyxan plant parasites (Phytomyxea) which, apart from three OTUs, were not represented in the forest ecosystem (Figure 2 and Supplementary Table S6). To our knowledge, this striking pattern was not observed to date, although Ferreira de Araujo et al (2018) noted that grassdominated ecosystems hosted more plant parasites than treedominated ones. The absence of Phytomyxea in temperate forests is corroborated by a recent metatranscriptomics study on leaf litter of 18 Biodiversity Exploratories forest sites (Voss et al, 2019), however, they were detected in low abundance in tropical forest soils (Mahé et al, 2017).…”

“…Because soil biota are incredibly diverse, they are commonly aggregated into feeding groups (guilds or trophic species) to facilitate the understanding of their complex interactions (Scheu, 2002). Protists make up a substantial fraction (30-40%) of the soil eukaryotes (Shen et al, 2014;Lanzén et al, 2016;Ferreira de Araujo et al, 2018), and have long been recognized as a pivotal component of soil food webs (Hunt et al, 1987). Despite this, they have only recently been included in general models of ecosystem services (de Vries et al, 2014), probably because of their immense diversity.…”

“…However, we are lacking baseline data on their occurrence in natural reservoirs, such as grasslands and forests (Stukenbrock and McDonald, 2008;van der Heijden et al, 2008). Cercozoa (Cavalier-Smith, 1998), a highly diverse phylum of c. 600 described species (Pawlowski et al, 2012), is a major protistan lineage in soil (Geisen et al, 2015;Grossmann et al, 2016;Lanzén et al, 2016;Ferreira de Araujo et al, 2018), comprising a vast array of functional traits in morphologies, nutrition and locomotive modes (Burki and Keeling, 2014). Recently the phylum Endomyxa was separated from Cercozoa (Bass et al, 2018;Cavalier-Smith et al, 2018), and it is of particular interest for containing inter alia plant pathogens of functional and economic significance, including important transmitters of plant viruses and agents of root tumors (e.g., club root disease) (Neuhauser et al, 2014;Bass et al, 2019).…”

Rhizosphere protists are key determinants of plant health

“…Specific linkages within co-occurrence networks only provide information about potential interactions, but further mechanistic proof for the interaction needs specific co-culture experiments. In addition to individual links, network structure and composition can provide insights about system's stability and increased potential for providing ecosystem services [37][38][39][40], suggesting that healthy plants benefit from the presence of a more complex network, among them higher numbers of phagotrophs (higher-trophic level organisms in general).…”