Phylogenetic and trophic determinants of gut microbiota in soil oribatid mites

Gong, Xin; Chen, Ting‐Wen; Zieger, Sarah L.; Bluhm, Sarah L.; Heidemann, Kerstin; Schaefer, Ina; Maraun, Mark; Liu, Manqiang; Scheu, Stefan

doi:10.1016/j.soilbio.2018.05.011

Cited by 15 publications

(10 citation statements)

References 62 publications

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“…The oxygen and water contents differed along the digestive tract of earthworms, thus the profile of microbiota is shaped by the digestive environment [ 34 – 36 ]. In addition, studies have revealed that the food source is another deterministic factor shaping the gut microbiome [ 37 – 40 ], both phylogeny and food preference of the host may deterministically shape the gut microbiome of soil animals [ 41 ]. For surviving in caves, earthworms therefore might select microbiota coding more metabolic activities.…”

Section: Discussionmentioning

confidence: 99%

Gut microbiome reflect adaptation of earthworms to cave and surface environments

et al. 2022

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Background Caves are special natural laboratories for most biota and the cave communities are unique. Establishing population in cave is accompanied with modifications in adaptability for most animals. To date, little is known about the survival mechanisms of soil animals in cave environments, albeit they play vital roles in most terrestrial ecosystems. Here, we investigated whether and how gut microbes would contribute to the adaptation of earthworms by comparing the gut microbiome of two earthworm species from the surface and caves. Results Two dominant earthworm species inhabited caves, i.e., Allolobophora chlorotica and Aporrectodea rosea. Compared with the counterparts on the surface, A. rosea significantly decreased population in the cave, while A. chlorotica didn’t change. Microbial taxonomic and phylogenetic diversities between the earthworm gut and soil environment were asynchronic with functional diversity, with functional gene diversity been always higher in earthworm gut than in soil, but species richness and phylogenetic diversity lower. In addition, earthworm gut microbiome were characterized by higher rrn operon numbers and lower network complexity than soil microbiota. Conclusions Different fitness of the two earthworm species in cave is likely to coincide with gut microbiota, suggesting interactions between host and gut microbiome are essential for soil animals in adapting to new environments. The functional gene diversity provided by gut microbiome is more important than taxonomic or phylogenetic diversity in regulating host adaptability. A stable and high-efficient gut microbiome, including microbiota and metabolism genes, encoded potential functions required by the animal hosts during the processes of adapting to and establishing in the cave environments. Our study also demonstrates how the applications of microbial functional traits analysis may advance our understanding of animal-microbe interactions that may aid animals to survive in extreme ecosystems.

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Section: Discussionmentioning

confidence: 99%

Gut microbiome reflect adaptation of earthworms to cave and surface environments

et al. 2022

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“…Among the taxa that shifted their diet significantly between beech and spruce forest there was only one primary decomposer (according to stable isotope data and enzyme activities; Maraun et al 2011;Siepel de Ruiter-Dijkman 1993), i.e., Achipteria coleoptrata. This species has limited ability to digest fungi (Gong et al 2018) and likely mainly feeds on dead plant material. However, in our study it also was associated with bacterial, fungal and plant FA markers indicating that it consumes a mixture of these resources.…”

Section: Trophic Plasticity Within Oribatid Mite Speciesmentioning

confidence: 99%

“…Eupelops hirtus, Eupelops plicatus and Liacarus xylariae have been assumed to be secondary decomposers, i.e., to mainly feeding on fungi (Maraun et al 2011;Gong et al 2018). In the present study, their food resources shifted from plants and fungi in the beech forest to bacteria and fungi in the spruce forest, suggesting that they are indeed secondary decomposers which are able to adapt to locally available resources.…”

Section: Trophic Plasticity Within Oribatid Mite Speciesmentioning

confidence: 99%

“…They feed on a wide variety of resources, ranging from dead organic material to lichens, algae, bacteria and fungi to nematodes (Maraun et al 2011). Their trophic ecology has been studied in the last decades using a variety of methods including stable isotope, fatty acid and molecular gut content analyses (Schneider et al 2004;Heidemann et al 2011;Pollierer et al 2012;Gong et al 2018). Fischer et al (2014) pointed out that the high variation in stable isotope signatures, as found in oribatid mites, points to trophic plasticity.…”

Section: Introductionmentioning

confidence: 99%

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Variation in trophic niches of oribatid mites in temperate forest ecosystems as indicated by neutral lipid fatty acid patterns

et al. 2020

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Shifting of trophic niches of soil microarthropods may allow them to adapt to changing resource conditions as induced by global change processes. However, the capability of microarthropods to shift their trophic niches is little studied. Whereas some studies based on stable isotopes ( 15 N/ 13 C) point to distinct and narrow trophic niches, others indicate that trophic niches are plastic. Here, we investigated shifts in trophic niches of oribatid mites (Oribatida, Acari), a major soil detritivore microarthropod group, due to forest management, i.e., plantation of beech and spruce forests in Central Europe, using neutral lipid fatty acid (NLFA) markers. Due to differential microbial communities, we expected a fungibased diet of oribatid mites in beech forest, but more bacterial contributions to the diet in spruce forest. Supporting these hypotheses, NLFA markers indicated that the trophic niches of each of the studied oribatid mite species differed between beech and spruce forests and shifted from feeding predominantly on litter and fungi in beech forest to more intensively feeding on bacteria in spruce forest. Oribatid mite species with the most pronounced differences in trophic niches included Achipteria coleoptrata, Eupelops hirtus, Eupelops plicatus and Liacarus xylariae, which had been classified as primary or secondary decomposers in previous studies. Overall, the results indicate that the ability of oribatid mite species to colonize different habitats and ecosystems is due to their ability to adjust their diet, i.e., to trophic plasticity. Changes in trophic niches in each of the studied oribatid mite species suggest that detritivores in soil may better cope with future changes in environmental conditions and associated changes in resource composition than species above the ground.

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“…In addition, understanding the assembly of microbial communities is critical in microbial ecology [ 21 – 23 ]. Previous studies have showed that substantial microbial variation occurs among individuals in the soil fauna microbiome [ 12 , 14 , 15 ]. However, few studies consider how microbial communities are assembled in the wild soil fauna.…”

Section: Introductionmentioning

confidence: 99%

Trophic level drives the host microbiome of soil invertebrates at a continental scale

et al. 2021

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Background Increasing our knowledge of soil biodiversity is fundamental to forecast changes in ecosystem functions under global change scenarios. All multicellular organisms are now known to be holobionts, containing large assemblages of microbial species. Soil fauna is now known to have thousands of species living within them. However, we know very little about the identity and function of host microbiome in contrasting soil faunal groups, across different terrestrial biomes, or at a large spatial scale. Here, we examined the microbiomes of multiple functionally important soil fauna in contrasting terrestrial ecosystems across China. Results Different soil fauna had diverse and unique microbiomes, which were also distinct from those in surrounding soils. These unique microbiomes were maintained within taxa across diverse sampling sites and in contrasting terrestrial ecosystems. The microbiomes of nematodes, potworms, and earthworms were more difficult to predict using environmental data, compared to those of collembolans, oribatid mites, and predatory mites. Although stochastic processes were important, deterministic processes, such as host selection, also contributed to the assembly of unique microbiota in each taxon of soil fauna. Microbial biodiversity, unique microbial taxa, and microbial dark matter (defined as unidentified microbial taxa) all increased with trophic levels within the soil food web. Conclusions Our findings demonstrate that soil animals are important as repositories of microbial biodiversity, and those at the top of the food web harbor more diverse and unique microbiomes. This hidden source of biodiversity is rarely considered in biodiversity and conservation debates and stresses the importance of preserving key soil invertebrates.

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Phylogenetic and trophic determinants of gut microbiota in soil oribatid mites

Cited by 15 publications

References 62 publications

Gut microbiome reflect adaptation of earthworms to cave and surface environments

Gut microbiome reflect adaptation of earthworms to cave and surface environments

Variation in trophic niches of oribatid mites in temperate forest ecosystems as indicated by neutral lipid fatty acid patterns

Trophic level drives the host microbiome of soil invertebrates at a continental scale

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