Unbalanced diets enhance the complexity of gut microbial network but destabilize its stability and resistance

Penghao Sun, Mengli Wang, Wei Zheng, Shuzhen Li, Xiaoyan Zhu, Xuejun Chai, Shanting Zhao

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 20. DOI: 10.1007/s44154-023-00098-x
Original Paper

Unbalanced diets enhance the complexity of gut microbial network but destabilize its stability and resistance

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Abstract

Stability is a fundamental ecological property of the gut microbiota and is associated with host health. Numerous studies have shown that unbalanced dietary components disturb the gut microbial composition and thereby contribute to the onset and progression of disease. However, the impact of unbalanced diets on the stability of the gut microbiota is poorly understood. In the present study, four-week-old mice were fed a plant-based diet high in refined carbohydrates or a high-fat diet for four weeks to simulate a persistent unbalanced diet. We found that persistent unbalanced diets significantly reduced the gut bacterial richness and increased the complexity of bacterial co-occurrence networks. Furthermore, the gut bacterial response to unbalanced diets was phylogenetically conserved, which reduced network modularity and enhanced the proportion of positive associations between community taxon, thereby amplifying the co-oscillation of perturbations among community species to destabilize gut microbial communities. The disturbance test revealed that the gut microbiota of mice fed with unbalanced diets was less resistant to antibiotic perturbation and pathogenic bacteria invasion. This study may fill a gap in the mechanistic understanding of the gut microbiota stability in response to diet and provide new insights into the gut microbial ecology.

Keywords

Diet / Gut microbiota / Community stability / Co-occurrence network

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Penghao Sun, Mengli Wang, Wei Zheng, Shuzhen Li, Xiaoyan Zhu, Xuejun Chai, Shanting Zhao. Unbalanced diets enhance the complexity of gut microbial network but destabilize its stability and resistance. Stress Biology, 2023, 3(1): 20 https://doi.org/10.1007/s44154-023-00098-x

References

[1]
AllesinaS, LevineJM. A competitive network theory of species diversity. Proc Natl Acad Sci U S A, 2011, 108(14):5638-5642
CrossRef Google scholar
[2]
AmendAS, MartinyAC, AllisonSD, BerlemontR, GouldenML, LuY, TresederKK, WeiheC, MartinyJB. Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. Isme j, 2016, 10(1):109-118
CrossRef Google scholar
[3]
BechtholdA, BoeingH, TetensI, SchwingshacklL, NöthlingsU. Perspective: food-based dietary guidelines in Europe-scientific concepts, current status, and perspectives. Adv Nutr, 2018, 9(5):544-560
CrossRef Google scholar
[4]
BlüherM. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol, 2019, 15(5):288-298
CrossRef Google scholar
[5]
BolyenE, RideoutJR, DillonMR, BokulichNA, AbnetCC, Al-GhalithGA, AlexanderH, AlmEJ, ArumugamM, AsnicarF, BaiY, BisanzJE, BittingerK, BrejnrodA, BrislawnCJ, BrownCT, CallahanBJ, Caraballo-RodríguezAM, ChaseJ, CopeEK, Da SilvaR, DienerC, DorresteinPC, DouglasGM, DurallDM, DuvalletC, EdwardsonCF, ErnstM, EstakiM, FouquierJ, GauglitzJM, GibbonsSM, GibsonDL, GonzalezA, GorlickK, GuoJ, HillmannB, HolmesS, HolsteH, HuttenhowerC, HuttleyGA, JanssenS, JarmuschAK, JiangL, KaehlerBD, KangKB, KeefeCR, KeimP, KelleyST, KnightsD, KoesterI, KosciolekT, KrepsJ, LangilleMGI, LeeJ, LeyR, LiuYX, LoftfieldE, LozuponeC, MaherM, MarotzC, MartinBD, McDonaldD, McIverLJ, MelnikAV, MetcalfJL, MorganSC, MortonJT, NaimeyAT, Navas-MolinaJA, NothiasLF, OrchanianSB, PearsonT, PeoplesSL, PetrasD, PreussML, PruesseE, RasmussenLB, RiversA, RobesonMS 2nd, RosenthalP, SegataN, ShafferM, ShifferA, SinhaR, SongSJ, SpearJR, SwaffordAD, ThompsonLR, TorresPJ, TrinhP, TripathiA, TurnbaughPJ, Ul-HasanS, van der HooftJJJ, VargasF, Vázquez-BaezaY, VogtmannE, von HippelM, WaltersW, WanY, WangM, WarrenJ, WeberKC, WilliamsonCHD, WillisAD, XuZZ, ZaneveldJR, ZhangY, ZhuQ, KnightR, CaporasoJG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37(8):852-857
CrossRef Google scholar
[6]
BuffieCG, PamerEG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol, 2013, 13(11):790-801
CrossRef Google scholar
[7]
BurnsAR, StephensWZ, StagamanK, WongS, RawlsJF, GuilleminK, BohannanBJ. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. Isme j, 2016, 10(3):655-664
CrossRef Google scholar
[8]
ByndlossMX, PernitzschSR, BäumlerAJ. Healthy hosts rule within: ecological forces shaping the gut microbiota. Mucosal Immunol, 2018, 11(5):1299-1305
CrossRef Google scholar
[9]
ChristA, LauterbachM, LatzE. Western diet and the immune system: an inflammatory connection. Immunity, 2019, 51(5):794-811
CrossRef Google scholar
[10]
CoyteKZ, SchluterJ, FosterKR. The ecology of the microbiome: networks, competition, and stability. Science, 2015, 350(6261):663-666
CrossRef Google scholar
[11]
de VriesFT, GriffithsRI, BaileyM, CraigH, GirlandaM, GweonHS, HallinS, KaisermannA, KeithAM, KretzschmarM, LemanceauP, LuminiE, MasonKE, OliverA, OstleN, ProsserJI, ThionC, ThomsonB, BardgettRD. Soil bacterial networks are less stable under drought than fungal networks. Nat Commun, 2018, 9(1):3033
CrossRef Google scholar
[12]
DengY, JiangYH, YangY, HeZ, LuoF, ZhouJ. Molecular ecological network analyses. BMC Bioinformatics, 2012, 13: 113
CrossRef Google scholar
[13]
DubinK, CallahanMK, RenB, KhaninR, VialeA, LingL, NoD, GobourneA, LittmannE, HuttenhowerC, PamerEG, WolchokJD. Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun, 2016, 7: 10391
CrossRef Google scholar
[14]
DunneJA, WilliamsRJ, MartinezND. Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci U S A, 2002, 99(20):12917-12922
CrossRef Google scholar
[15]
DuránP, ThiergartT, Garrido-OterR, AglerM, KemenE, Schulze-LefertP, HacquardS. Microbial Interkingdom interactions in roots promote arabidopsis survival. Cell, 2018, 175(4):973-983.e914
CrossRef Google scholar
[16]
FassarellaM, BlaakEE, PendersJ, NautaA, SmidtH, ZoetendalEG. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health. Gut, 2021, 70(3):595-605
CrossRef Google scholar
[17]
FaustK, RaesJ. Microbial interactions: from networks to models. Nat Rev Microbiol, 2012, 10(8):538-550
CrossRef Google scholar
[18]
FlintHJ, DuncanSH, LouisP. The impact of nutrition on intestinal bacterial communities. Curr Opin Microbiol, 2017, 38: 59-65
CrossRef Google scholar
[19]
FosterKR, SchluterJ, CoyteKZ, Rakoff-NahoumS. The evolution of the host microbiome as an ecosystem on a leash. Nature, 2017, 548(7665):43-51
CrossRef Google scholar
[20]
GanguliS, PalS, DasK, BanerjeeR, BagchiSS. Gut microbial dataset of a foraging tribe from rural West Bengal - insights into unadulterated and transitional microbial abundance. Data Brief, 2019, 25: 103963
CrossRef Google scholar
[21]
GillSR, PopM, DeboyRT, EckburgPB, TurnbaughPJ, SamuelBS, GordonJI, RelmanDA, Fraser-LiggettCM, NelsonKE. Metagenomic analysis of the human distal gut microbiome. Science, 2006, 312(5778):1355-1359
CrossRef Google scholar
[22]
GravelD, MassolF, LeiboldMA. Stability and complexity in model meta-ecosystems. Nat Commun, 2016, 7: 12457
CrossRef Google scholar
[23]
HallKD, GuoJ, CourvilleAB, BoringJ, BrychtaR, ChenKY, DarceyV, FordeCG, GharibAM, GallagherI, HowardR, JosephPV, MilleyL, OuwerkerkR, RaisingerK, RozgaI, SchickA, StaglianoM, TorresS, WalterM, WalterP, YangS, ChungST. Effect of a plant-based, low-fat diet versus an animal-based, ketogenic diet on ad libitum energy intake. Nat Med, 2021, 27(2):344-353
CrossRef Google scholar
[24]
HammarlundSP, HarcombeWR. Refining the stress gradient hypothesis in a microbial community. Proc Natl Acad Sci U S A, 2019, 116(32):15760-15762
CrossRef Google scholar
[25]
HernandezDJ, DavidAS, MengesES, SearcyCA, AfkhamiME. Environmental stress destabilizes microbial networks. Isme j, 2021, 15(6):1722-1734
CrossRef Google scholar
[26]
HerrenCM, McMahonKD. Cohesion: a method for quantifying the connectivity of microbial communities. Isme j, 2017, 11(11):2426-2438
CrossRef Google scholar
[27]
IsobeK, AllisonSD, KhaliliB, MartinyAC, MartinyJBH. Phylogenetic conservation of bacterial responses to soil nitrogen addition across continents. Nat Commun, 2019, 10(1):2499
CrossRef Google scholar
[28]
Le ChatelierE, NielsenT, QinJ, PriftiE, HildebrandF, FalonyG, AlmeidaM, ArumugamM, BattoJM, KennedyS, LeonardP, LiJ, BurgdorfK, GrarupN, JørgensenT, BrandslundI, NielsenHB, JunckerAS, BertalanM, LevenezF, PonsN, RasmussenS, SunagawaS, TapJ, TimsS, ZoetendalEG, BrunakS, ClémentK, DoréJ, KleerebezemM, KristiansenK, RenaultP, Sicheritz-PontenT, de VosWM, ZuckerJD, RaesJ, HansenT, BorkP, WangJ, EhrlichSD, PedersenO. Richness of human gut microbiome correlates with metabolic markers. Nature, 2013, 500(7464):541-546
CrossRef Google scholar
[29]
LiY, ZhangT, ShiM, ZhangB, HuX, XuS, DingJ, LiuS, HuD, RubensteinD. Characterization of intestinal microbiota and fecal cortisol, T3, and IgA in forest musk deer (Moschus berezovskii) from birth to weaning. Integ Zool, 2021, 16(3):300-312
CrossRef Google scholar
[30]
LiuC, CuiY, LiX, YaoM. microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol, 2021, 97(2):fiaa255
CrossRef Google scholar
[31]
LiuTC, KernJT, JainU, SonnekNM, XiongS, SimpsonKF, VanDussenKL, WinklerES, HarituniansT, MaliqueA, LuQ, SasakiY, StorerC, DiamondMS, HeadRD, McGovernDPB, StappenbeckTS. Western diet induces paneth cell defects through microbiome alterations and farnesoid X receptor and type I interferon activation. Cell Host Microbe, 2021, 29(6):988-1001.e1006
CrossRef Google scholar
[32]
Lloyd-PriceJ, Abu-AliG, HuttenhowerC. The healthy human microbiome. Genome Med, 2016, 8(1):51
CrossRef Google scholar
[33]
LozuponeCA, StombaughJI, GordonJI, JanssonJK, KnightR. Diversity, stability and resilience of the human gut microbiota. Nature, 2012, 489(7415):220-230
CrossRef Google scholar
[34]
Ludwig DS, Ebbeling CB (2018) The carbohydrate-insulin model of obesity: beyond “Calories In, Calories Out.” JAMA Intern Med 178(8):1098–1103. https://doi.org/10.1001/jamainternmed.2018.2933
[35]
MakkiK, DeehanEC, WalterJ, BäckhedF. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Mic, 2018, 23(6):705-715
CrossRef Google scholar
[36]
MardinogluA, WuH, BjornsonE, ZhangC, HakkarainenA, RäsänenSM, LeeS, MancinaRM, BergentallM, PietiläinenKH, SöderlundS, MatikainenN, StåhlmanM, BerghPO, AdielsM, PieningBD, GranérM, LundbomN, WilliamsKJ, RomeoS, NielsenJ, SnyderM, UhlénM, BergströmG, PerkinsR, MarschallHU, BäckhedF, TaskinenMR, BorénJ. An integrated understanding of the rapid metabolic benefits of a carbohydrate-restricted diet on hepatic steatosis in humans. Cell Metab, 2018, 27(3):559-571.e555
CrossRef Google scholar
[37]
MartinyAC, TresederK, PuschG. Phylogenetic conservatism of functional traits in microorganisms. Isme j, 2013, 7(4):830-838
CrossRef Google scholar
[38]
MartinyJB, JonesSE, LennonJT, MartinyAC. Microbiomes in light of traits: a phylogenetic perspective. Science, 2015, 350(6261):aac9323
CrossRef Google scholar
[39]
McHardyIH, GoudarziM, TongM, RueggerPM, SchwagerE, WegerJR, GraeberTG, SonnenburgJL, HorvathS, HuttenhowerC, McGovernDP, FornaceAJ Jr, BornemanJ, BraunJ. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome, 2013, 1(1):17
CrossRef Google scholar
[40]
Michalska-SmithM, SongZ, Spawn-LeeSA, HansenZA, JohnsonM, MayG, BorerET, SeabloomEW, KinkelLL. Network structure of resource use and niche overlap within the endophytic microbiome. Isme j, 2022, 16(2):435-446
CrossRef Google scholar
[41]
Morais LH, Schreiber HLt, Mazmanian SK (2021) The gut microbiota-brain axis in behaviour and brain disorders. Nat Rev Microbiol 19:(4)241-255. doi:https://doi.org/10.1038/s41579-020-00460-0
[42]
MorrisseyEM, MauRL, SchwartzE, CaporasoJG, DijkstraP, van GestelN, KochBJ, LiuCM, HayerM, McHughTA, MarksJC, PriceLB, HungateBA. Phylogenetic organization of bacterial activity. Isme j, 2016, 10(9):2336-2340
CrossRef Google scholar
[43]
MougiA, KondohM. Diversity of interaction types and ecological community stability. Science, 2012, 337(6092):349-351
CrossRef Google scholar
[44]
NeutelAM, HeesterbeekJA, De RuiterPC. Stability in real food webs: weak links in long loops. Science (New York, NY), 2002, 296(5570):1120-1123
CrossRef Google scholar
[45]
OlesenJM, BascompteJ, DupontYL, JordanoP. The modularity of pollination networks. Proceed Natl Acad Sci U S A, 2007, 104(50):19891-19896
CrossRef Google scholar
[46]
OrtizA, VegaNM, RatzkeC, GoreJ. Interspecies bacterial competition regulates community assembly in the C. elegans intestine. Isme j, 2021, 15(7):2131-2145
CrossRef Google scholar
[47]
PapenfortK, BasslerBL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol, 2016, 14(9):576-588
CrossRef Google scholar
[48]
RaymondF, OuameurAA, DéraspeM, IqbalN, GingrasH, DridiB, LeprohonP, PlantePL, GirouxR, BérubéÈ, FrenetteJ, BoudreauDK, SimardJL, ChabotI, DomingoMC, TrottierS, BoissinotM, HuletskyA, RoyPH, OuelletteM, BergeronMG, CorbeilJ. The initial state of the human gut microbiome determines its reshaping by antibiotics. The ISME J, 2016, 10(3):707-720
CrossRef Google scholar
[49]
RelmanDA. The human microbiome: ecosystem resilience and health. Nutr Rev, 2012, 70 Suppl 1(Suppl 1):S2-9
CrossRef Google scholar
[50]
RöttjersL, FaustK. From hairballs to hypotheses-biological insights from microbial networks. FEMS Microbiol Rev, 2018, 42(6):761-780
CrossRef Google scholar
[51]
SonnenburgJL, BäckhedF. Diet-microbiota interactions as moderators of human metabolism. Nature, 2016, 535(7610):56-64
CrossRef Google scholar
[52]
SporA, KorenO, LeyR. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol, 2011, 9(4):279-290
CrossRef Google scholar
[53]
StoufferDB, BascompteJ. Compartmentalization increases food-web persistence. Proc Natl Acad Sci U S A, 2011, 108(9):3648-3652
CrossRef Google scholar
[54]
SunP, WangM, LiZ, WeiJ, LiuF, ZhengW, ZhuX, ChaiX, ZhaoS. Eucommiae cortex polysaccharides mitigate obesogenic diet-induced cognitive and social dysfunction via modulation of gut microbiota and tryptophan metabolism (Research Paper). Theranostics, 2022, 12(8):3637-3655
CrossRef Google scholar
[55]
TakahashiK, SuzukiN, OgraY. Effect of gut microflora on nutritional availability of selenium. Food Chem, 2020, 319: 126537
CrossRef Google scholar
[56]
ValdesAM, WalterJ, SegalE, SpectorTD. Role of the gut microbiota in nutrition and health. BMJ (Clinical research ed), 2018, 361: k2179
CrossRef Google scholar
[57]
Wali JA, Milner AJ, Luk AWS, Pulpitel TJ, Dodgson T, Facey HJW, Wahl D, Kebede MA, Senior AM, Sullivan MA, Brandon AE, Yau B, Lockwood GP, Koay YC, Ribeiro R, Solon-Biet SM, Bell-Anderson KS, O’Sullivan JF, Macia L, Forbes JM, Cooney GJ, Cogger VC, Holmes A, Raubenheimer D, Le Couteur DG, Simpson SJ (2021) Impact of dietary carbohydrate type and protein-carbohydrate interaction on metabolic health. Nat Metab 3(6):810–828. https://doi.org/10.1038/s42255-021-00393-9
[58]
WuGD, ChenJ, HoffmannC, BittingerK, ChenYY, KeilbaughSA, BewtraM, KnightsD, WaltersWA, KnightR, SinhaR, GilroyE, GuptaK, BaldassanoR, NesselL, LiH, BushmanFD, LewisJD. Linking long-term dietary patterns with gut microbial enterotypes. Science, 2011, 334(6052):105-108
CrossRef Google scholar
[59]
YooW, ZiebaJK, FoegedingNJ, TorresTP, SheltonCD, ShealyNG, ByndlossAJ, CevallosSA, GertzE, TiffanyCR, ThomasJD, LitvakY, NguyenH, OlsanEE, BennettBJ, RathmellJC, MajorAS, BäumlerAJ, ByndlossMX. High-fat diet-induced colonocyte dysfunction escalates microbiota-derived trimethylamine N-oxide. Science (New York, NY), 2021, 373(6556):813-818
CrossRef Google scholar
[60]
YuanMM, GuoX, WuL, ZhangY, XiaoN, NingD, ShiZ, ZhouX, WuL, YangY, TiedjeJM, ZhouJ. Climate warming enhances microbial network complexity and stability. Nat Climate Change, 2021, 11(4):343-348
CrossRef Google scholar
[61]
ZelezniakA, AndrejevS, PonomarovaO, MendeDR, BorkP, PatilKR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci U S A, 2015, 112(20):6449-6454
CrossRef Google scholar

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