Changes in Trophic Groups of Protists With Conversion of Rainforest Into Rubber and Oil Palm Plantations

Abstract

Protists, abundant but enigmatic single-celled eukaryotes, are important soil microbiota providing numerous ecosystem functions. We employed high-throughput sequencing of environmental DNA, targeting the V4 region of the 18S rRNA gene, to characterize changes in their abundance, species richness, and community structure with conversion of lowland rainforest into rubber agroforest (jungle rubber), and rubber and oil palm plantations; typical agricultural systems in Sumatra, Indonesia. We identified 5,204 operational taxonomic units (OTUs) at 97% identity threshold of protists from 32 sites. Protists species richness was similar in rainforest, jungle rubber and oil palm plantations but significantly lower in rubber plantations. After standardization, 4,219 OTUs were assigned to five trophic groups, and inspected for effects of land-use change, and potential biotic and abiotic driving factors. The most abundant trophic group was phagotrophs (52%), followed by animal parasites (29%), photoautotrophs (12%), plant parasites (1%), and symbionts (<1%). However, the relative abundance and OTU richness of phagotrophs and photoautotrophs increased significantly with increasing land-use intensity. This was similar, but less pronounced, for the relative abundance of symbionts. Animal and plant parasites decreased significantly in abundance and species richness with increasing land-use intensity. Community compositions and factors affecting the structure of individual trophic groups differed between land-use systems. Parasites were presumably mainly driven by the abundance and species richness of their hosts, while phagotrophs by changes in soil pH and increase in Gram-positive bacteria, and photoautotrophs by light availability. Overall, the results show that relative species richness, relative abundance, and community composition of individual trophic groups of protists in tropical lowland rainforest significantly differ from that in converted ecosystems. This is likely associated with changes in ecosystem functioning. The study provides novel insight into protist communities and their changes with land-use intensity in tropical lowland ecosystems. We show, that trophic groups of protists are powerful indicators reflecting changes in the functioning of ecosystems with conversion of rainforest into monoculture plantations.

Unravelling the effects of tropical land use conversion on the soil microbiome

“…Increasing abundances along the land use gradient from rainforest to converted systems were also observed for Chaetothyriales and Pleosporales with p.adj < 0.05 in Bukit rubber samples. We compared trophic groups of protists in each land use system (0.09% of all reads) using the same functional categories described by Schulz et al [10] (Additional file 4: Figure S3). Phagotrophs were the most abundant group (37 to 39%) followed by photoautotrophs (29 to 30%) and animal parasites (27 to 31%).…”

“…Composition of different trophic protist groups. Trophic groups were assigned according to Schulz et al [10]. Compositions are displayed for each land use in the respective landscape as relative abundances.…”

“…In addition, microorganisms play a key role in decomposing soil organic matter and mineralizing nutrients in soil [7]. It has been shown that rainforest conversion to plantations has negative effects on the biodiversity of fungi [8,9], protists [10], vertebrates [11], insects and plants [12][13][14], archaea [15], but not on bacterial diversity which increased [15,16]. Additionally, the microbial community composition was severely affected by these conversion processes with a high impact on Proteobacteria which showed an abundance decrease and Actinobacteria, which showed an abundance increase with increasing land use intensity [15,16].…”

“…We linked functional results with their corresponding taxonomic background. Based on our previous studies analysing the 16S rRNA marker gene sequences in the same sampling sites and studies on similar systems in Southeast Asia [9,10,15,16,18,33], we formulated three hypotheses. We assume that diversity will decrease for soilborne archaea, Eukaryotes and increase for bacteria with increasing land use intensity (H1).…”

Contrasting responses of protistan plant parasites and phagotrophs to ecosystems, land management and soil properties

“…Even less is known about the distribution of protistan plant pathogens in natural habitats: most of the protists that are known to interact with plants belong to the Stramenopiles-Alveolata-Rhizaria super group (Harosa or "SAR" ), particularly those belonging to oomycetes (Stramenopiles) and Cercozoa (Rhizaria) (Hassani et al, 2018). For example, Schulz et al (2019), investigating a gradient of land use intensification from tropical rain forest to plantations, reported significant shifts in the composition of protistan phagotrophs, phototrophs and plant pathogens. A study under controlled greenhouse conditions showed a reduction of the relative abundance of plant pathogenic protists was reduced by organic fertilizer amendments, while bacterivores and omnivores increased (Xiong et al, 2018).…”