1. Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China 2. School of Geographical Sciences, Fujian Normal University, Fuzhou 350007, China 3. Institute of Plant Nutrition, Resources and Environment, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China 4. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China 5. Cangzhou Academy of Agricultural and Forestry Sciences, Hebei Key Laboratory of Soil Entomology, Cangzhou 061001, China
● Microbial attributes were compared between soil fauna gut and plant rhizosphere.
● Manure applications decreased or increased gut or rhizosphere bacterial diversity.
● Stochastic or deterministic processes drove gut or rhizosphere bacterial assembly.
● Manure applications increased bacterial network complexity of gut and rhizosphere.
Diverse microbes inhabit animals and plants, helping their hosts perform multiple functions in agricultural ecosystems. However, the responses of soil fauna gut and plant rhizosphere microbiomes to livestock manure applications are still not well understood. Here we fed Protaetia brevitarsis larvae (PBL) with chicken manure and collected their frass. The frass and manure were applied as fertilizers to lettuce pots. We then compared the changes of microbial diversity, community assembly, and potential functions between the gut group (i.e., all PBL gut and frass samples) and the rhizosphere group (i.e., all rhizosphere soil samples). We revealed that manure applications (i.e., feeding or fertilization) decreased bacterial diversity in the gut group but increased that in the rhizosphere group. Particularly, the proportions of Bacilli in the gut group and Gammaproteobacteria in the rhizosphere group were increased (up to a maximum of 33.8% and 20.4%, respectively) after manure applications. Stochastic and deterministic processes dominated community assembly in the gut and rhizosphere microbiomes, respectively. Manure applications increased the microbial co-occurrence network complexity of both the gut and rhizosphere groups. Moreover, the proportions of functional taxa associated with human/animal pathogens in the gut group and carbon/nitrogen cycling in the rhizosphere group were enhanced (up to 2.6-fold and 24.6-fold, respectively). Our findings illustrate the different responses of microbial diversity, community assembly, and potential functions in soil fauna gut and plant rhizosphere to manure applications. The results could enhance our knowledge on the reasonable utilization of animal and plant microbiomes in agricultural management.
M., Bastian, S., Heymann, M., Jacomy, 2009. Gephi: an open source software for exploring and manipulating networks. Proceedings of the International AAAI Conference on Web and Social Media3, 361–362. https://doi.org/10.1609/icwsm.v3i1.13937
2
S., Bhunia, A., Bhowmik, R., Mallick, J., Mukherjee, 2021. Agronomic efficiency of animal-derived organic fertilizers and their effects on biology and fertility of soil: A review. Agronomy (Basel)11, 823. https://doi.org/10.3390/agronomy11050823
M., Bonkowski, C., Villenave, B., Griffiths, 2009. Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant and Soil321, 213–233. https://doi.org/10.1007/s11104-009-0013-2
5
M., Bradford, T.H., Jones, R.D., Bardgett, H.I., Black, B., Boag, M., Bonkowski, R., Cook, T., Eggers, A., Gange, S., Grayston, E., Kandeler, A.E., McCaig, J.E., Newington, J.I., Prosser, H., Setälä, P.L., Staddon, G.M., Tordoff, D., Tscherko, J.H., Lawton, 2002. Impacts of soil faunal community composition on model grassland ecosystems. Science298, 615–618. https://doi.org/10.1126/science.1075805
6
D., Bulgarelli, M., Rott, K., Schlaeppi, E., Ver Loren van Themaat, N., Ahmadinejad, F., Assenza, P., Rauf, B., Huettel, R., Reinhardt, E., Schmelzer, J., Peplies, F.O., Gloeckner, R., Amann, T., Eickhorst, P., Schulze-Lefert, 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature488, 91–95. https://doi.org/10.1038/nature11336
7
J.G., Caporaso, J., Kuczynski, J., Stombaugh, K., Bittinger, F.D., Bushman, E.K., Costello, N., Fierer, A.G., Pena, J.K., Goodrich, J.I., Gordon, G.A., Huttley, S.T., Kelley, D., Knights, J.E., Koenig, R.E., Ley, C.A., Lozupone, D., McDonald, B.D., Muegge, M., Pirrung, J., Reeder, J.R., Sevinsky, P.J., Tumbaugh, W.A., Walters, J., Widmann, T., Yatsunenko, J., Zaneveld, R., Knight, 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336. https://doi.org/10.1038/nmeth.f.303
8
J.G., Caporaso, C.L., Lauber, W.A., Walters, D., Berg-Lyons, C.A., Lozupone, P.J., Turnbaugh, N., Fierer, R., Knight, 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America108, 4516–4522. https://doi.org/10.1073/pnas.1000080107
9
A.E., Cazemier, J.C., Verdoes, F.A., Reubsaet, J.H., Hackstein, C., van der Drift, H.J., Op den Camp, 2003. Promicromonospora pachnodae sp. nov., a member of the (hemi) cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata. Antonie van Leeuwenhoek83, 135–148. https://doi.org/10.1023/A:1023325817663
10
D.C., Coleman, D.H., Wall, 2015. Soil fauna: Occurrence, biodiversity, and roles in ecosystem function. Soil Microbiology Ecology and Biochemistry4, 111–149.
11
G., Csardi, T., Nepusz, 2006. The igraph software package for complex network research. InterJournal Complex Systems1695, 1–9.
R.C., Edgar, 2016. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257
16
M.C., Enebe, O.O., Babalola, 2021. Soil fertilization affects the abundance and distribution of carbon and nitrogen cycling genes in the maize rhizosphere. AMB Express11, 1–10. https://doi.org/10.1186/s13568-021-01182-z
17
P., Engel, N.A., Moran, 2013. The gut microbiota of insects−diversity in structure and function. FEMS Microbiology Reviews37, 699–735. https://doi.org/10.1111/1574-6976.12025
18
M., Fassarella, E.E., Blaak, J., Penders, A., Nauta, H., Smidt, E.G., Zoetendal, 2021. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health. Gut70, 595–605. https://doi.org/10.1136/gutjnl-2020-321747
19
C.R., Fitzpatrick, I., Salas-González, J.M., Conway, O.M., Finkel, S., Gilbert, D., Russ, P.J.P.L., Teixeira, J.L., Dangl, 2020. The plant microbiome: from ecology to reductionism and beyond. Annual Review of Microbiology74, 81–100. https://doi.org/10.1146/annurev-micro-022620-014327
20
S., Hacquard, R., Garrido-Oter, A., González, S., Spaepen, G., Ackermann, S., Lebeis, A.C., McHardy, J.L., Dangl, R., Knight, R., Ley, P., Schulze-Lefert, 2015. Microbiota and host nutrition across plant and animal kingdoms. Cell Host & Microbe17, 603–616. https://doi.org/10.1016/j.chom.2015.04.009
21
N.E., Hamilton, M., Ferry, 2018. ggtern: Ternary diagrams using ggplot2. Journal of Statistical Software87, 1–17. https://doi.org/10.18637/jss.v087.c03
22
S.E., Hannula, F., Zhu, R., Heinen, T.M., Bezemer, 2019. Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nature Communications10, 1254. https://doi.org/10.1038/s41467-019-09284-w
23
S.W., Huang, H.Y., Zhang, S., Marshall, T.A., Jackson, 2010. The scarab gut: A potential bioreactor for bio-fuel production. Insect Science17, 175–183. https://doi.org/10.1111/j.1744-7917.2010.01320.x
24
S., Jiao, Y., Yang, Y., Xu, J., Zhang, Y., Lu, 2020. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME Journal14, 202–216. https://doi.org/10.1038/s41396-019-0522-9
25
P., Kardol, M.A., Cregger, C.E., Campany, A.T., Classen, 2010. Soil ecosystem functioning under climate change: plant species and community effects. Ecology91, 767–781. https://doi.org/10.1890/09-0135.1
26
R., Kolde, 2012. Pheatmap: pretty heatmaps. R package version1, 747.
27
P., Langfelder, S., Horvath, 2012. Fast R functions for robust correlations and hierarchical clustering. Journal of Statistical Software46, 1–17. https://doi.org/10.18637/jss.v046.i11
28
P., Lavelle, 1996. Diversity of soil fauna and ecosystem function. Biology International33, 1–16.
29
H.Z., Li, D., Zhu, J.H., Lindhardt, S.M., Lin, X., Ke, L., Cui, 2021. Long-term fertilization history alters effects of microplastics on soil properties, microbial communities, and functions in diverse farmland ecosystem. Environmental Science & Technology55, 4658–4668. https://doi.org/10.1021/acs.est.0c04849
D., Liu, B., Lian, C., Wu, P., Guo, 2018. A comparative study of gut microbiota profiles of earthworms fed in three different substrates. Symbiosis74, 21–29. https://doi.org/10.1007/s13199-017-0491-6
32
S., Louca, L.W., Parfrey, M., Doebeli, 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277. https://doi.org/10.1126/science.aaf4507
33
F., Luo, J., Zhong, Y., Yang, R.H., Scheuermann, J., Zhou, 2006. Application of random matrix theory to biological networks. Physics Letters. [Part A]357, 420–423. https://doi.org/10.1016/j.physleta.2006.04.076
L.W., Mendes, E.E., Kuramae, A.A., Navarrete, J.A., Van Veen, S.M., Tsai, 2014. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME Journal8, 1577–1587. https://doi.org/10.1038/ismej.2014.17
36
R., Mendes, J.M., Raaijmakers, 2015. Cross-kingdom similarities in microbiome functions. ISME Journal9, 1905–1907. https://doi.org/10.1038/ismej.2015.7
37
D.B., Müller, C., Vogel, Y., Bai, J.A., Vorholt, 2016. The plant microbiota: systems-level insights and perspectives. Annual Review of Genetics50, 211–234. https://doi.org/10.1146/annurev-genet-120215-034952
38
J., Oksanen, F.G., Blanchet, R., Kindt, P., Legendre, P., Minchin, R., O'Hara, G., Simpson, P., Solymos, M., Henry, M., Stevens, 2015. Vegan: community ecology package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. R package ver, 2.3–1
39
J.M., Pickard, M.Y., Zeng, R., Caruso, G., Núñez, 2017. Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunological Reviews279, 70–89. https://doi.org/10.1111/imr.12567
40
S.T., Ramírez-Puebla, L.E., Servín-Garcidueñas, B., Jiménez-Marín, L.M., Bolaños, M., Rosenblueth, J., Martínez, M.A., Rogel, E., Ormeño-Orrillo, E., Martínez-Romero, 2013. Gut and root microbiota commonalities. Applied and Environmental Microbiology79, 2–9. https://doi.org/10.1128/AEM.02553-12
41
S., Schreiter, G.C., Ding, H., Heuer, G., Neumann, M., Sandmann, R., Grosch, S., Kropf, K., Smalla, 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Frontiers in Microbiology5, 144. https://doi.org/10.3389/fmicb.2014.00144
J.C., Stegen, X., Lin, J.K., Fredrickson, X., Chen, D.W., Kennedy, C.J., Murray, M.L., Rockhold, A., Konopka, 2013. Quantifying community assembly processes and identifying features that impose them. ISME Journal7, 2069–2079. https://doi.org/10.1038/ismej.2013.93
44
Y., Sun, D., Snow, H., Walia, X., Li, 2021. Transmission routes of the microbiome and resistome from manure to soil and lettuce. Environmental Science & Technology55, 11102–11112. https://doi.org/10.1021/acs.est.1c02985
45
Team, R.C., 2013. R: A language and environment for statistical computing
46
A., Tkacz, J., Cheema, G., Chandra, A., Grant, P.S., Poole, 2015. Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. ISME Journal9, 2349–2359. https://doi.org/10.1038/ismej.2015.41
47
K., Wang, P., Gao, L., Geng, C., Liu, J., Zhang, C., Shu, 2022a. Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line. Microbiome10, 1–16. https://doi.org/10.1186/s40168-022-01291-2
48
Y.F., Wang, P., Chen, F.H., Wang, W.X., Han, M., Qiao, W.X., Dong, C.S., Hu, D., Zhu, H.Y., Chu, Y.G., Zhu, 2022b. The ecological clusters of soil organisms drive the ecosystem multifunctionality under long-term fertilization. Environment International161, 107133. https://doi.org/10.1016/j.envint.2022.107133
49
T., Whitman, R., Neurath, A., Perera, I., Chu-Jacoby, D., Ning, J., Zhou, P., Nico, J., Pett‐Ridge, M., Firestone, 2018. Microbial community assembly differs across minerals in a rhizosphere microcosm. Environmental Microbiology20, 4444–4460. https://doi.org/10.1111/1462-2920.14366
Q., Xiang, D., Zhu, Q.L., Chen, M., Delgado-Baquerizo, J.Q., Su, M., Qiao, X.R., Yang, Y.G., Zhu, 2019. Effects of diet on gut microbiota of soil collembolans. Science of the Total Environment676, 197–205. https://doi.org/10.1016/j.scitotenv.2019.04.104
52
C., Xiong, B.K., Singh, J.Z., He, Y.L., Han, P.P., Li, L.H., Wan, G.Z., Meng, S.Y., Liu, J.T., Wang, C.F., Wu, A.H., Ge, L.M., Zhang, 2021. Plant developmental stage drives the differentiation in ecological role of the maize microbiome. Microbiome9, 1–15. https://doi.org/10.1186/s40168-021-01118-6
L., Xu, M., Yi, H., Yi, E., Guo, A., Zhang, 2018. Manure and mineral fertilization change enzyme activity and bacterial community in millet rhizosphere soils. World Journal of Microbiology & Biotechnology34, 1–13. https://doi.org/10.1007/s11274-017-2394-3
55
X., Zhang, R., Zhang, J., Gao, X., Wang, F., Fan, X., Ma, H., Yin, C., Zhang, K., Feng, Y., Deng, 2017. Thirty-one years of rice-rice-green manure rotations shape the rhizosphere microbial community and enrich beneficial bacteria. Soil Biology & Biochemistry104, 208–217. https://doi.org/10.1016/j.soilbio.2016.10.023
56
Y., Zhang, X., Hao, T.W., Alexander, B.W., Thomas, X., Shi, N.Z., Lupwayi, 2018. Long-term and legacy effects of manure application on soil microbial community composition. Biology and Fertility of Soils54, 269–283. https://doi.org/10.1007/s00374-017-1257-2
57
J., Zhao, G., Duan, Y., Zhu, D., Zhu, 2023. Gut microbiota and transcriptome response of earthworms (Metaphire guillelmi) to polymyxin B exposure. Journal of Environmental Sciences (China)133, 37–47. https://doi.org/10.1016/j.jes.2022.07.033
58
X., Zhao, J.P., Shen, C.L., Shu, S.S., Jin, H.J., Di, L.M., Zhang, J.Z., He, 2022. Attenuation of antibiotic resistance genes in livestock manure through vermicomposting via Protaetia brevitarsis and its fate in a soil-vegetable system. Science of the Total Environment807, 150781. https://doi.org/10.1016/j.scitotenv.2021.150781
59
F., Zheng, X., Mou, J., Zhang, T., Zhang, L., Xia, S., Yin, L., Wu, X., Leng, S., An, D., Zhao, 2022a. Gradual enhancement of the assemblage stability of the reed rhizosphere microbiome with recovery time. Microorganisms10, 937. https://doi.org/10.3390/microorganisms10050937
J., Zhou, Y., Deng, P., Zhang, K., Xue, Y., Liang, J.D., Van Nostrand, Y., Yang, Z., He, L., Wu, D.A., Stahl, T.C., Hazen, J.M., Tiedje, A.P., Arkin, 2014. Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proceedings of the National Academy of Sciences of the United States of America111, E836–E845. https://doi.org/10.1073/pnas.1324044111
62
D., Zhu, M., Delgado-Baquerizo, J., Ding, M.R., Gillings, Y.G., Zhu, 2021. Trophic level drives the host microbiome of soil invertebrates at a continental scale. Microbiome9, 1–16. https://doi.org/10.1186/s40168-021-01144-4
