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Disentangling Diet- and Medium-Associated Microbes in Shaping Daphnia Gut Microbiome

  • Host Microbe Interactions
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Abstract

Host genotype and environment are considered crucial factors in shaping Daphnia gut microbiome composition. Among the environmental factors, diet is an important factor that regulates Daphnia microbiome. Most of the studies only focused on the use of axenic diet and non-sterile medium to investigate their effects on Daphnia microbiome. However, in natural environment, Daphnia diets such as phytoplankton are associated with microbes and could affect Daphnia microbiome composition and fitness, but remain relatively poorly understood compared to that of axenic diet. To test this, we cultured two Daphnia magna genotypes (genotype-1 and genotype-2) in sterile medium and fed with axenic diet. To check the effects of algal diet-associated microbes versus free water-related microbes, Daphnia were respectively inoculated with three different inoculums: medium microbial inoculum, diet-associated microbial inoculum, and medium and diet-mixed microbial inoculum. Daphnia were cultured for 3 weeks and their gut microbiome and life history traits were recorded. Results showed that Daphnia inoculated with medium microbial inoculum were dominated by Comamonadaceae in both genotypes. In Daphnia inoculated with mixed inoculum, genotype-1 microbiome was highly changed, whereas genotype-2 microbiome was slightly altered. Daphnia inoculated with diet microbial inoculum has almost the same microbiome in both genotypes. The total number of neonates and body size were significantly reduced in Daphnia inoculated with diet microbial inoculum regardless of genotype compared to all other treatments. Overall, this study shows that the microbiome of Daphnia is flexible and varies with genotype and diet- and medium-associated microbes, but not every bacteria is beneficial to Daphnia, and only symbionts can increase Daphnia performance.

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Data Availability

Sequence data is deposited in the Sequence Read Database (SRA) and available online under BioProject PRJNA737109. All other data will be available when requested.

Code Availability

Not applicable.

References

  1. Sommer F, Bäckhed F (2013) The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11:227–238. https://doi.org/10.1038/nrmicro2974

    Article  CAS  PubMed  Google Scholar 

  2. Adair KL, Douglas AE (2017) Making a microbiome: the many determinants of host-associated microbial community composition. Curr Opin Microbiol 35:23–29. https://doi.org/10.1016/j.mib.2016.11.002

    Article  PubMed  Google Scholar 

  3. Peixoto RS, Harkins DM, Nelson KE (2021) Advances in microbiome research for animal health. Microb Ecol 9:289–311. https://doi.org/10.1146/annurev-animal-091020-075907

    Article  CAS  Google Scholar 

  4. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267. https://doi.org/10.1126/science.1223813

    Article  CAS  PubMed  Google Scholar 

  5. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215. https://doi.org/10.1126/science.1188235

    Article  CAS  PubMed  Google Scholar 

  6. Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci 108:19288–19292. https://doi.org/10.1073/pnas.1110474108

    Article  PubMed  PubMed Central  Google Scholar 

  7. Erica VH, Jacobus CR, Nicole MG (2019) Diet–microbiome–disease: investigating diet’s influence on infectious disease resistance through alteration of the gut microbiome. PLoS Pathog. 15(10):e1007891. https://doi.org/10.1371/journal.ppat.1007891

    Article  CAS  Google Scholar 

  8. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290. https://doi.org/10.1038/nrmicro2540

    Article  CAS  PubMed  Google Scholar 

  9. Frankel-Bricker J, Song MJ, Benner MJ, Schaack S (2019) Variation in the microbiota associated with Daphnia magna across genotypes, populations, and temperature. Microb Ecol 79:731–742. https://doi.org/10.1007/s00248-019-01412-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Jackrel SL, Schmidt KC, Cardinale BJ, Denef VJ (2020) Microbiomes reduce their host’s sensitivity to interspecific interactions. mBio 11:e02657-19. https://doi.org/10.1128/mbio.02657-19

    Article  PubMed  PubMed Central  Google Scholar 

  11. Taipale SJ, Brett MT, Pulkkinen K, Kainz MJ (2012) The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction, and lipid composition. FEMS Microbiol Ecol 82:50–62. https://doi.org/10.1111/j.1574-6941.2012.01406.x

    Article  CAS  PubMed  Google Scholar 

  12. Lyu K, Guan H, Wu C, Wang X, Wilson AE, Yang Z (2016) Maternal consumption of non-toxic Microcystis by Daphnia magna induces tolerance to toxic Microcystis in offspring. Freshw Biol 61:219–228. https://doi.org/10.1111/fwb.12695

    Article  CAS  Google Scholar 

  13. Lyu K, Cao C, Li D, Akbar S, Yang Z (2021) The thermal regime modifies the response of aquatic keystone species Daphnia to microplastics: evidence from population fitness, accumulation, histopathological analysis and candidate gene expression. Sci Total Environ 783:147154. https://doi.org/10.1016/j.scitotenv.2021.147154

    Article  CAS  PubMed  Google Scholar 

  14. Huang J, Li YR, Zhou QM, Sun YF, Zhang L, Gu L, Lyu K, Huang Y, Chen YF, Yang Z (2020) Non-toxic and toxic Microcystis aeruginosa reduce the tolerance of Daphnia pulex to low calcium in different degrees: based on the changes in the key life-history traits. Chemosphere 248:226101. https://doi.org/10.1016/j.chemosphere.2020.126101

    Article  CAS  Google Scholar 

  15. Yang Z, Xiang F, Minter EJA, Lü K, Chen Y, Montagnes DJS (2011) The interactive effects of microcystin and nitrite on life-history parameters of the cladoceran Daphnia obtusa. J Hazard Mater 190:113–118. https://doi.org/10.1016/j.jhazmat.2011.03.002

    Article  CAS  PubMed  Google Scholar 

  16. Akbar S, Du JJ, Jia Y, Tian XJ (2017) The importance of calcium in improving resistance of Daphnia to Microcystis. PLoS ONE 12:e0175881. https://doi.org/10.1371/journal.pone.0175881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bovyn RA, McCauley E, LaMontagne JM (2018) Offspring size-number tradeoffs and food quality feedbacks impact population dynamics in a Daphnia-algae system. Oikos 127:1152–1162. https://doi.org/10.1111/oik.04788

    Article  Google Scholar 

  18. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG, Svanbäck R (2014) Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17:979–987. https://doi.org/10.1111/ele.12301

    Article  PubMed  PubMed Central  Google Scholar 

  19. Derrien M, Veiga P (2017) Rethinking diet to aid human-microbe symbiosis. Trends Microbiol 25:100–112. https://doi.org/10.1016/j.tim.2016.09.011

    Article  CAS  PubMed  Google Scholar 

  20. Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065. https://doi.org/10.1038/nmicrobiol.2017.65

    Article  CAS  PubMed  Google Scholar 

  21. Schmidt KC, Jackrel SL, Smith DJ, Dick GJ, Denef VJ (2020) Genotype and host microbiome alter competitive interactions between Microcystis aeruginosa and Chlorella sorokiniana. Harmful Algae 99:101939. https://doi.org/10.1016/j.hal.2020.101939

    Article  CAS  PubMed  Google Scholar 

  22. Jackrel SL, Yang JW, Schmidt KC, Denef VJ (2021) Host specificity of microbiome assembly and its fitness effects in phytoplankton. ISME J 15:774–788. https://doi.org/10.1038/s41396-020-00812-x

    Article  PubMed  Google Scholar 

  23. Johnson AJ, Zheng JJ, Kang JW, Saboe A, Knights D & Zivkovic AM (2020) A guide to diet-microbiome study design. Front Nutr 7. https://doi.org/10.3389/fnut.2020.00079

  24. Zhang X, Ohtsuki H, Makino W, Kato Y, Watanabe H, Urabe J (2021) Variations in effects of ectosymbiotic microbes on the growth rates among different species and genotypes of Daphnia fed different algal diets. Ecol Res 36:303–312. https://doi.org/10.1111/1440-1703.12194

    Article  CAS  Google Scholar 

  25. Sullam KE, Pichon S, Schaer TMM, Ebert D (2018) The combined effect of temperature and host clonal line on the microbiota of a planktonic crustacean. Microb Ecol 76:506–517. https://doi.org/10.1007/s00248-017-1126-4

    Article  CAS  PubMed  Google Scholar 

  26. Callens M, Watanabe H, Kato Y, Miura J, Decaestecker E (2018) Microbiota inoculum composition affects holobiont assembly and host growth in Daphnia. Microbiome 6:56. https://doi.org/10.1186/s40168-018-0444-1

    Article  PubMed  PubMed Central  Google Scholar 

  27. Callens M, Macke E, Muylaert K, Bossier P, Lievens B, Waud M, Decaestecker E (2015) Food availability affects the strength of mutualistic host-microbiota interactions in Daphnia magna. ISME J 10:911–920. https://doi.org/10.1038/ismej.2015.166

    Article  PubMed  PubMed Central  Google Scholar 

  28. Mushegian AA, Ebert D (2017) Presence of microbiota reverses the relative performance of Daphnia on two experimental diets. Zoology 125:29–31. https://doi.org/10.1016/j.zool.2017.07.007

    Article  PubMed  Google Scholar 

  29. Cooper RO, Cressler CE (2020) Characterization of key bacterial species in the Daphnia magna microbiota using shotgun metagenomics. Sci Rep 10:652. https://doi.org/10.1038/s41598-019-57367-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Macke E, Callens M, De Meester L, Decaestecker E (2017) Host-genotype dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nat Commu 8:1608. https://doi.org/10.1038/s41467-017-01714-x

    Article  CAS  Google Scholar 

  31. Smith DJ, Tan JY, Powers MA, Lin XN, Davis TW, Dick GJ (2021) Individual Microcystis colonies harbour distinct bacterial communities that differ by Microcystis oligotype and with time. Environ Microbiol. https://doi.org/10.1111/1462-2920.15514

    Article  PubMed  Google Scholar 

  32. Cirri E, Pohnert G (2019) Algae-bacteria interactions that balance the planktonic microbiome. New Phytol 223:100–106. https://doi.org/10.1111/nph.15765

    Article  PubMed  Google Scholar 

  33. Akbar S, Gu L, Sun YF, Zhou QM, Zhang L, Lyu K, Yuan H, Yang Z (2020) Changes in the life history traits of Daphnia magna are associated with the gut microbiota composition shaped by diet and antibiotics. Sci Total Environ 705:135827. https://doi.org/10.1016/j.scitotenv.2019.135827

    Article  CAS  PubMed  Google Scholar 

  34. Akbar S, Huang J, Zhou QM, Gu L, Sun YF, Zhang L, Lyu K, Yang Z (2021) Elevated temperature and toxic Microcystis reduce Daphnia fitness and modulate gut microbiota. Environ Pollut 271:116409. https://doi.org/10.1016/j.envpol.2020.116409

    Article  CAS  PubMed  Google Scholar 

  35. Cooper RO, Vavra JM, Cressler CE (2021) Targeted manipulation of abundant and rare taxa in the Daphnia magna microbiota with antibiotics impacts host fitness differentially. mSystems 6:e00916-20. https://doi.org/10.1128/msystems.00916-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Eckert EM, Anicic N, Fontaneto D (2021) Freshwater zooplankton microbiome composition is highly flexible and strongly influenced by the environment. Mol Ecol 30:1545–1558. https://doi.org/10.1111/mec.15815

    Article  PubMed  Google Scholar 

  37. Freese HM, Schink B (2011) Composition and stability of the microbial community inside the digestive tract of the aquatic crustacean Daphnia magna. Microb Ecol 62:882–894. https://doi.org/10.1007/s00248-011-9886-8

    Article  PubMed  Google Scholar 

  38. Eigemann F, Hilt S, Salka I, Grossart HP (2013) Bacterial community composition associated with freshwater algae: species specificity vs. dependency on environmental conditions and source community. FEMS Microbiol Ecol 83:650–663. https://doi.org/10.1111/1574-6941.12022

    Article  CAS  PubMed  Google Scholar 

  39. Foster KR, Schluter J, Coyte KZ, Rakoff-Nahoum S (2017) The evolution of the host microbiome as an ecosystem on a leash. Nature 548:43–51. https://doi.org/10.1038/nature23292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mushegian AA, Walser JC, Sullam KE, Ebert D (2018) The microbiota of diapause: how host-microbe associations are formed after dormancy in an aquatic crustacean. J Anim Ecol 87:400–413. https://doi.org/10.1111/1365-2656.12709

    Article  PubMed  Google Scholar 

  41. Peerakietkhajorn S, Tsukada K, Kato Y, Matsuura T, Watanabe H (2015) Symbiotic bacteria contribute to increasing the population size of a freshwater crustacean, Daphnia magna. Environ Microbiol Rep 7:364–372. https://doi.org/10.1111/1758-2229.12260

    Article  CAS  PubMed  Google Scholar 

  42. Marinho MC, Lage OM, Catita J, Antunes SC (2018) Adequacy of planctomycetes as supplementary food source for Daphnia magna. Antonie Van Leeuwenhoek 111:825–840. https://doi.org/10.1007/s10482-017-0997-1

    Article  CAS  PubMed  Google Scholar 

  43. Sison-Mangus MP, Mushegian AA, Ebert D (2015) Water fleas require microbiota for survival, growth and reproduction. ISME J 9:59–67. https://doi.org/10.1038/ismej.2014.116

    Article  PubMed  Google Scholar 

  44. Ruuskanen MO, Sommeria-Klein G, Havulinna AS, Niiranen TJ, Lahti L (2021) Modelling spatial patterns in host-associated microbial communities. Environ Microbiol 23:2374–2388. https://doi.org/10.1111/1462-2920.15462

    Article  PubMed  Google Scholar 

  45. Grainger TN, Letten AD, Gilbert B, Fukami T (2019) Applying modern coexistence theory to priority effects. Proc Natl Acad Sci 116:6205–6210. https://doi.org/10.1073/pnas.1803122116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Li WZ, Nelson KE (2021) Microbial species that initially colonize the human gut at birth or in early childhood can stay in human body for lifetime. Microb Ecol. https://doi.org/10.1007/s00248-020-01636-0

    Article  PubMed  PubMed Central  Google Scholar 

  47. Callens M, De Meester L, Muylaert K, Mukherjee S, Decaestecker E (2020) The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community. FEMS Microbiol Ecol 96. https://doi.org/10.1093/femsec/fiaa128

  48. Houwenhuyse S, Stoks R, Mukherjee S, Decaestecker E (2021) Locally adapted gut microbiomes host stress tolerance. ISME J. https://doi.org/10.1038/s41396-021-00940-y

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (31730105 and 31800385), China Postdoctoral Science Foundation (2020M681658), and the Priority Academic Program Development of Jiangsu Higher Education Institutions of China.

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Authors and Affiliations

  1. Jiangsu Key Laboratory for Biodiversity and Biotechnology, School of Biological Sciences, Nanjing Normal University, 1 Wenyuan Road, Nanjing, 210023, China

    Siddiq Akbar, Xianxian Li, Zihao Ding, Qi Liu, Jing Huang, Qiming Zhou, Lei Gu & Zhou Yang

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  1. Siddiq Akbar
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  2. Xianxian Li
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  3. Zihao Ding
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  4. Qi Liu
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  8. Zhou Yang
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Contributions

S.A and Z.Y conceptualize and designed the present study. S.A, Q.L, X.L, L.G, and Z.D performed experiments. S.A, J.H, and Q.Z analyzed the data. S.A wrote the manuscript. S.A and Z.Y revised and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Zhou Yang.

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Akbar, S., Li, X., Ding, Z. et al. Disentangling Diet- and Medium-Associated Microbes in Shaping Daphnia Gut Microbiome. Microb Ecol 84, 911–921 (2022). https://doi.org/10.1007/s00248-021-01900-x

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