Abstract
Aims
Bacterial communities inhabiting seeds may interact not only with the plant host, but also with seed predators. The study compared the bacterial communities associated with seeds of seven weeds Crepis biennis, Taraxacum officinale, Tripleurospermum inodorum, Plantago lanceolata, Thlaspi arvense, Silene latifolia and Leonurus cardiaca, after burial in soil for two years, and demonstrated how these changes relate to seed mass, viability and attractiveness for a seed predator, Pseudoophonus rufipes (DeGeer) (Coleoptera: Carabidae).
Results
Bacterial diversity, assessed by Illumina MiSeq sequencing of the 16S rRNA amplicon, increased 5–10 times, while seed viability and mass decreased with burial time. Mostly, the seed species differed in their microbiomes and changes in seed properties together with their attractiveness to the beetle. Seed microbiomes remained specific after burial and contained taxa characteristic for both plant endophytes but also insect guts. In all seeds, 5 zero radius OTUs (ZOTU) were common after one year of burial, while only one common ZOTU remained after the second year. Seeds of T. officinale and T. inodorum lost attractiveness for the beetle approx. by 90 and 80% resp., while seeds of T. arvense improved their attractiveness by 80% after soil exposure. Changes in seed consumption were partially explained by bacterial communities and seed properties, namely the C/N ratio and seed viability.
Conclusions
Seed mass, viability, C/N and beetle predation were related to the bacterial community. These relationships also changed after seed burial in soil, which may impact seed survival and consequently influence plant population dynamics and weed management.
Similar content being viewed by others
References
Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego
Bastian F, Bouziri L, Nicolardot B, Ranjard L (2009) Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biol Biochem 41:262–275. https://doi.org/10.1016/j.soilbio.2008.10.024
Bekker RM, Knevel IC, Tallowin JBR et al (1998) Soil nutrient input effects on seed longevity: a burial experiment with fen-meadow species. Funct Ecol 12:673–682. https://doi.org/10.1046/j.1365-2435.1998.00238.x
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Blankenchip CL, Michels DE, Elizabeth Braker H, Goffredi SK (2018) Diet breadth and exploitation of exotic plants shift the core microbiome of Cephaloleia, a group of tropical herbivorous beetles. PeerJ 6:e4793. https://doi.org/10.7717/peerj.4793
Borza JK, Westerman PR, Liebman M (2007) Comparing estimates of seed viability in three foxtail (Setaria) species using the imbibed seed crush test with and without additional tetrazolium testing. Weed Technol 21:518–522. https://doi.org/10.1614/wt-06-110
Bredon M, Depuydt E, Brisson L et al (2021) Effects of dysbiosis and dietary manipulation on the digestive microbiota of a detritivorous arthropod. Microorganisms 9:1–15. https://doi.org/10.3390/microorganisms9010148
Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522. https://doi.org/10.1073/pnas.1000080107
Chee-Sanford J, Fu X (2010) Investigating the role of microorganisms in soil seed bank management. In: Mendez-Vilas A (ed) Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Formatex, Badajoz, pp 257–66
Chen D, Chen X, Jia C et al (2021) Effects of precipitation and microorganisms on persistence of buried seeds: a case study of 11 species from the Loess Plateau of China. Plant Soil. https://doi.org/10.1007/s11104-021-04990-1
Colman DR, Toolson EC, Takacs-Vesbach CD (2012) Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 21:5124–5137. https://doi.org/10.1111/j.1365-294X.2012.05752.x
D’Alessandro M, Erb M, Ton J et al (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant, Cell Environ 37:813–826. https://doi.org/10.1111/pce.12220
Dalling JW, Davis AS, Schutte BJ, Elizabeth Arnold A (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95. https://doi.org/10.1111/j.1365-2745.2010.01739.x
Davis AS, Cardina J, Forcella F et al (2005) Environmental factors affecting seed persistence of annual weeds across the U.S. corn belt. Weed Sci 53:860–868. https://doi.org/10.1614/ws-05-064r1.1
Davis AS, Fu X, Schutte BJ et al (2016) Interspecific variation in persistence of buried weed seeds follows trade-offs among physiological, chemical, and physical seed defenses. Ecol Evol 6:6836–6845. https://doi.org/10.1002/ece3.2415
Douglas GM, Maffei VJ, Zaneveld JR et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
Durán P, Thiergart T, Garrido-Oter R et al (2018) Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175:973-983.e14. https://doi.org/10.1016/j.cell.2018.10.020
Ebert KM, Arnold WG, Ebert PR, Merritt DJ (2021) Hindgut microbiota reflects different digestive strategies in dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Appl Environ Microbiol 87:e02100-20. https://doi.org/10.1128/AEM.02100-20
Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv 081257. https://doi.org/10.1101/081257
Engel P, Moran NA (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev 37:699–735
Ernst F, Shetty S, Borman T, Lahti L (2022) mia: Microbiome analysis. R package version 1.2.7. https://github.com/microbiome/mia
Escobar Rodríguez C, Mitter B, Barret M et al (2018) Commentary: seed bacterial inhabitants and their routes of colonization. Plant Soil 422:129–134. https://doi.org/10.1007/s11104-017-3368-9
Escobar Rodríguez C, Antonielli L, Mitter B et al (2020) Heritability and functional importance of the Setaria viridis bacterial seed microbiome. Phytobiomes J 4:40–52. https://doi.org/10.1094/PBIOMES-04-19-0023-R
Evans MEG, Forsythe TG (1985) Feeding mechanisms, and their variation in form, of some adult ground-beetles (Coleoptera: Caraboidea). J Zool 206:113–143. https://doi.org/10.1111/J.1469-7998.1985.TB05640.X
Foffová H, Ćavar Zeljković SZ, Honěk A et al (2020) Which seed properties determine the preferences of carabid beetle seed predators? Insects 11:1–13. https://doi.org/10.3390/insects11110757
Frank AC, Guzmán JPS, Shay JE (2017) Transmission of bacterial endophytes. Microorganisms 5. https://doi.org/10.3390/microorganisms5040070
Gardarin A, Dürr C, Mannino MR et al (2010) Seed mortality in the soil is related to seed coat thickness. Seed Sci Res 20:243–256. https://doi.org/10.1017/S0960258510000255
Gee GW, Bauder JW (1986) Particle-size Analysis. In: Klute A (ed) Methods of Soil Analysis, Part I: Physical and Mineralogical Methods. American Society of Agronomy-Soil Science Society of America, Madison, pp 383–411
Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/mmbr.00050-14
Hodkinson DJ, Askew AP, Thompson K et al (1998) Ecological correlates of seed size in the British flora. Funct Ecol 12:762–766. https://doi.org/10.1046/j.1365-2435.1998.00256.x
Honek A, Martinkova Z, Jarosik V (2003) Ground beetles (Carabidae) as seed predators. Eur J Entomol 100:531–544. https://doi.org/10.14411/eje.2003.081
Honek A, Martinkova Z, Saska P, Pekar S (2007) Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera). Basic Appl Ecol 8:343–353. https://doi.org/10.1016/j.baae.2006.07.002
Hou C, Shi Y, Wang H et al (2018) Composition and diversity analysis of intestinal microbiota in the fifth instar silkworm, Bombyx mori L. Invertebr Surviv J 15:223–233. https://doi.org/10.25431/1824-307X/isj.v15i1.223-233
Hubová P, Tejnecký V, Češková M et al (2018) Behaviour of aluminium in forest soils with different lithology and herb vegetation cover. J Inorg Biochem 181:139–144. https://doi.org/10.1016/J.JINORGBIO.2017.09.017
Ihnen K, Zimmer M (2008) Selective consumption and digestion of litter microbes by Porcellio scaber (Isopoda: Oniscidea). Pedobiologia (Jena) 51:335–342. https://doi.org/10.1016/j.pedobi.2007.06.001
Jang S, Kikuchi Y (2020) Impact of the insect gut microbiota on ecology, evolution, and industry. Curr Opin Insect Sci 41:33–39. https://doi.org/10.1016/j.cois.2020.06.004
Johnston-Monje D, Lundberg DS, Lazarovits G et al (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405:337–355. https://doi.org/10.1007/s11104-016-2826-0
Jones RT, Sanchez LG, Fierer N (2013) A cross-taxon analysis of insect-associated bacterial diversity. PLoS One 8:e61218. https://doi.org/10.1371/journal.pone.0061218
Kong HG, Song GC, Ryu CM (2019) Inheritance of seed and rhizosphere microbial communities through plant–soil feedback and soil memory. Environ Microbiol Rep 11:479–486. https://doi.org/10.1111/1758-2229.12760
Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Kuchta K, Volk RB, Rauwald HW (2013) Stachydrine in Leonurus cardiaca, Leonurus japonicus, Leonotis leonurus: Detection and quantification by instrumental HPTLC and 1H-qNMR analyses. Pharmazie 68:534–540. https://doi.org/10.1691/ph.2013.6527
Kulkarni SS, Dosdall LM, Willenborg CJ (2015) The role of ground beetles (Coleoptera: Carabidae) in weed seed consumption: a review. Weed Sci 63:355–376. https://doi.org/10.1614/ws-d-14-00067.1
Larios L, Pearson DE, Maron JL (2017) Incorporating the effects of generalist seed predators into plant community theory. Funct Ecol 31:1856–1867
Links MG, Demeke T, Gräfenhan T et al (2014) Simultaneous profiling of seed-associated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds. New Phytol 202:542–553. https://doi.org/10.1111/nph.12693
Long RL, Steadman KJ, Panetta FD, Adkins SW (2009) Soil type does not affect seed ageing when soil water potential and temperature are controlled. Plant Soil 320:131–140. https://doi.org/10.1007/s11104-008-9878-8
Long RL, Gorecki MJ, Renton M et al (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev 90:31–59. https://doi.org/10.1111/brv.12095
Lundgren JG, Lehman RM (2010) Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle. PLoS One 5:e10831. https://doi.org/10.1371/journal.pone.0010831
Lundgren JG, Rosentrater KA (2007) The strength of seeds and their destruction by granivorous insects. Arthropod Plant Interact 1:93–99. https://doi.org/10.1007/s11829-007-9008-1
Martinková Z, Saska P, Honěk A (2006) Consumption of fresh and buried seed by ground beetles (Coleoptera: Carabidae). Eur J Entomol 103:361–364. https://doi.org/10.14411/eje.2006.048
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297. https://doi.org/10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
Miller EC, Perron GG, Collins CD (2019) Plant-driven changes in soil microbial communities influence seed germination through negative feedbacks. Ecol Evol 9:9298–9311. https://doi.org/10.1002/ece3.5476
Moreira X, Abdala-Roberts L, Bruun HH et al (2021) Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species. Ann Bot 125:881–890. https://doi.org/10.1093/AOB/MCZ207
Müller-Stöver D, Nybroe O, Baraibar B et al (2016) Contribution of the seed microbiome to weed management. Weed Res 56:335–339. https://doi.org/10.1111/wre.12218
Nelson EB, Simoneau P, Barret M et al (2018) Editorial special issue: the soil, the seed, the microbes and the plant. Plant Soil 422:1–5. https://doi.org/10.1007/s11104-018-3576-y
Nikolić N, Squartini A, Concheri G et al (2020) Weed seed decay in no-till field and planted riparian buffer zone. Plants 9:293. https://doi.org/10.3390/plants9030293
Pakeman RJ, Small JL, Torvell L (2012) Edaphic factors influence the longevity of seeds in the soil. Plant Ecol 213:57–65. https://doi.org/10.1007/s11258-011-0006-0
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org
Rahman M, Liu L, Barkla BJ (2021) A single seed protein extraction protocol for characterizing Brassica seed storage proteins. Agronomy 11:107. https://doi.org/10.3390/agronomy11010107
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
Rybakova D, Cernava T, Köberl M et al (2016) Endophytes-assisted biocontrol: novel insights in ecology and the mode of action of Paenibacillus. Plant Soil 405:125–140. https://doi.org/10.1007/s11104-015-2526-1
Sagova-Mareckova M, Cermak L, Novotna J et al (2008) Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Appl Environ Microbiol 74:2902–2907. https://doi.org/10.1128/AEM.02161-07
Samreen T, Naveed M, Nazir MZ et al (2021) Seed associated bacterial and fungal endophytes: Diversity, life cycle, transmission, and application potential. Appl Soil Ecol 168:104191. https://doi.org/10.1016/j.apsoil.2021.104191
Saska P (2008) Effect of diet on the fecundity of three carabid beetles. Physiol Entomol 33:188–192. https://doi.org/10.1111/j.1365-3032.2008.00618.x
Saska P, Koprdová S, Martinková Z, Honěk A (2014) Comparing methods of weed seed exposure to predators. Ann Appl Biol 164:301–312. https://doi.org/10.1111/aab.12102
Saska P, Honěk A, Foffová H, Martinková Z (2019a) Burial-induced changes in the seed preferences of carabid beetles (Coleoptera: Carabidae). Eur J Entomol 116:133–140. https://doi.org/10.14411/EJE.2019.015
Saska P, Honěk A, Martinková Z (2019b) Preferences of carabid beetles (Coleoptera: Carabidae) for herbaceous seeds. Acta Zool Acad Sci Hungaricae 65:57–76. https://doi.org/10.17109/AZH.65.SUPPL.57.2019
Saska P, Foffová H, Martinková Z, Honěk A (2020) Persistence and changes in morphological traits of herbaceous seeds due to burial in soil. Agronomy 10:1–16. https://doi.org/10.3390/agronomy10030448
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Schmid RB, Lehman RM, Brözel VS, Lundgren JG (2015) Gut bacterial symbiont diversity within beneficial insects linked to reductions in local biodiversity. Ann Entomol Soc Am 108:993–999. https://doi.org/10.1093/aesa/sav081
Schutte BJ, Davis AS, Peinado SA, Ashigh J (2014) Seed-coat thickness data clarify seed size-seed-bank persistence trade-offs in Abutilon theophrasti (Malvaceae). Seed Sci Res 24:119–131. https://doi.org/10.1017/S0960258514000099
Segers FH, Kešnerová L, Kosoy M, Engel P (2017) Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. https://doi.org/10.1038/ismej.2016.201
Sharma P, Kumar T, Yadav M et al (2021) Plant-microbe interactions for the sustainable agriculture and food security. Plant Gene 28:100325. https://doi.org/10.1016/j.plgene.2021.100325
Singh BK, Liu H, Trivedi P (2020) Eco-holobiont: A new concept to identify drivers of host-associated microorganisms. Environ Microbiol 22:564–567. https://doi.org/10.1111/1462-2920.14900
Tannenbaum I, Kaur J, Mann R et al (2020) Profiling the Lolium perenne microbiome: from seed to seed. Phytobiomes J 4:281–289. https://doi.org/10.1094/PBIOMES-03-20-0026-R
Tejnecký V, Drábek O, Nikodem A et al (2014) Fast determination of water extractable organic carbon from forest soils. Zpravy Lesn Vyzk 59:155–159
Thompson K, Band SR, Hodgson JG (1993) Seed size and shape predict persistence in soil. Funct Ecol 7:236–241
Thompson K, Bakker JP, Bekker RM (1997) The soil seed banks of North West Europe: Methodology, density and longevity. Cambridge University Press, Cambridge
Thompson K, Bakker JP, Bekker RM, Hodgson JG (1998) Ecological correlates of seed persistence in soil in the north-west European flora. J Ecol 86:163–169. https://doi.org/10.1046/j.1365-2745.1998.00240.x
Torres-Cortés G, Bonneau S, Bouchez O et al (2018) Functional microbial features driving community assembly during seed germination and emergence. Front Plant Sci 9:1–16. https://doi.org/10.3389/fpls.2018.00902
Trognitz F, Hackl E, Widhalm S, Sessitsch A (2016) The role of plant-microbiome interactions in weed establishment and control. FEMS Microbiol Ecol 92:1–15. https://doi.org/10.1093/femsec/fiw138
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: Genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50. https://doi.org/10.1111/1758-2229.12181
Vacheron J, Péchy-Tarr M, Brochet S et al (2019) T6SS contributes to gut microbiome invasion and killing of an herbivorous pest insect by plant-beneficial Pseudomonas protegens. ISME J 13:1318–1329. https://doi.org/10.1038/s41396-019-0353-8
Van Mourik TA, Stomph TJ, Murdoch AJ (2005) Why high seed densities within buried mesh bags may overestimate depletion rates of soil seed banks. J Appl Ecol 42:299–305. https://doi.org/10.1111/j.1365-2664.2005.01016.x
van Overbeek LS, Franke AC, Nijhuis EHM et al (2011) Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microb Ecol 62:257–264. https://doi.org/10.1007/s00248-011-9845-4
Vandenkoornhuyse P, Quaiser A, Duhamel M et al (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206. https://doi.org/10.1111/nph.13312
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Wang Y, Rozen DE (2017) Gut microbiota colonization and Nicrophorus vespilloides throughout development. Appl Environ Microbiol 83:1–13
WRB (2015) World reference base for soil resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. Rome
Yilma G, Bekele M (2021) The role of soil bacteria in the control of parasitic Striga hermonthica weed. Int J Adv Res Biol Sci 8:12–20. https://doi.org/10.22192/ijarbs.2021.08.05.002
Yilmaz P, Parfrey LW, Yarza P et al (2014) The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:D643–D648. https://doi.org/10.1093/nar/gkt1209
Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda: Oniscidea): an evolutionary-ecological approach. Biol Rev Camb Philos Soc 77:455–493. https://doi.org/10.1017/S1464793102005912
Zytynska SE, Meyer ST (2019) Effects of biodiversity in agricultural landscapes on the protective microbiome of insects – a review. Entomol Exp Appl 167:2–13. https://doi.org/10.1111/eea.12751
Acknowledgements
We wish to thank Jana Kohoutová, Hana Smutná and Iveta Slaninová for their help with seed preparation and sample processing. The work was supported by the Czech Science Foundation project #14-02773S, Ministry of Agriculture of the CR, project QK1810370 and institutional project RO 0418, and by Ministry of Education, Youth and Sports of the Czech Republic, European Regional Development Fund-Project CZ.02.1.01/0.0/0.0/16_019/0000845. Finally, we would like to thank Dr. Keith Edwards for English editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Anna Maria Pirttila.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Saska, P., Kopecky, J., Omelka, M. et al. Seed properties and bacterial communities are associated with feeding preferences of a seed-eating beetle. Plant Soil 480, 329–348 (2022). https://doi.org/10.1007/s11104-022-05584-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05584-1