Bacterial community network complexity and role of stochasticity decrease during primary succession

Highlights

● Bacterial networks became less connected with soil development along primary succession.

● Community composition was initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with decreasing pH.

● Most natural microorganisms in extreme habitats exist as consortia that provide robustness and extensive metabolic capabilities in structuring bacterial communities.

Abstract

In microbial ecology, there is limited understanding of the mechanisms governing patterns in community structure across space and time. Here, we studied the changes of bacterial co-occurrence network structure over four primary successional soils after glacier retreat, including a sand dune system and three glacier foreland series, varying in timescale from centuries to millennia. We found that in all series, network structure was most complex in the earliest stages of succession, and became simpler over time. Richness and abundance of keystone species and network stability also declined over time. It appears that with less productive, nutrient poor and physiologically extreme conditions of early succession, closer interactions among bacterial species are ecologically selected for. These may take the form of consortia (with positive interactions) or stronger niche exclusion (with negative interactions). Additionally, we quantified the relative roles of different structuring processes on bacterial community using a bin-based null model analysis (iCAMP). With each successional series, community composition was initially governed by stochasticity, but as succession proceeded there was a progressive increase in deterministic selection over time, correlated with decreasing pH. Overall, our results show a consistency among the four series in long-term processes of community succession, with more integrated networks and greater stochasticity in early stages.

Key words： glacial retreat; bacteria; chronosequence; co-occurrence network; 16S rRNA sequencing; community assembly

Declaration of competing interest

The authors declare no conflict of interest.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0218-y and is accessible for authorized users.

References

1 Aslani, F., Geisen, S., Ning, D., Tedersoo, L., Bahram, M., 2022. Towards revealing the global diversity and community assembly of soil eukaryotes. Ecology Letters25, 65–76.

2 Bahl, J., Lau, M.C., Smith, G.J., Vijaykrishna, D., Cary, S.C., Lacap, D.C., Lee, C.K., Papke, R.T., Warren-Rhodes, K.A., Wong, F.K.Y., McKay, C.P., Pointing, S.B., 2011. Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nature Communications2, 163.

3 Banerjee, S., Kirkby, C.A., Schmutter, D., Bissett, A., Kirkegaard, J.A., Richardson, A.E., 2016. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biology & Biochemistry97, 188–198.

4 Banerjee, S., Schlaeppi, K., van der Heijden, M.G.A., 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology16, 567–576.

5 Barberan, A., Bates, S.T., Casamayor, E.O., Fierer, N., 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME Journal6, 343–351.

6 Belnap, J., Harper, K.T., Warren, S.D., 1993. Surface disturbance of cryptobiotic soil crusts: Nitrogenase activity, chlorophyll content, and chlorophyll degradation. Arid Soil Research and Rehabilitation8, 1–8.

7 Berry, D., Widder, S., 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Frontiers in Microbiology5, 219.

8 Bolhuis, H., Stal, L.J., 2011. Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME Journal5, 1701–1712.

9 Brankatschk, R., Towe, S., Kleineidam, K., Schloter, M., Zeyer, J., 2011. Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield. ISME Journal5, 1025–1037.

10 Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336.

11 Caruso, T., Chan, Y., Lacap, D.C., Lau, M.C.Y., McKay, C.P., Pointing, S.B., 2011. Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME Journal5, 1406–1413.

12 Chase, J.M., 2007. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences of the United States of America104, 17430–17434.

13 Chen, B., Jiao, S., Luo, S., Ma, B., Qi, W., Cao, C., Zhao, Z., Du, G., Ma, X., 2021. High soil pH enhances the network interactions among bacterial and archaeal microbiota in alpine grasslands of the Tibetan Plateau. Environmental Microbiology23, 464–477.

14 Chu, H., Fierer, N., Lauber, C.L., Caporaso, J.G., Knight, R., Grogan, P., 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environmental Microbiology12, 2998–3006.

15 Ciccazzo, S., Esposito, A., Borruso, L., Brusetti, L., 2016. Microbial communities and primary succession in high altitude mountain environments. Annals of Microbiology66, 43–60.

16 Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., Smith, A.G., 2005. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature438, 90–93.

17 Cumming, G.S., Bodin, Ö., Ernstson, H., Elmqvist, T., 2010. Network analysis in conservation biogeography: challenges and opportunities. Diversity & Distributions16, 414–425.

18 Cutler, N.A., Chaput, D.L., van der Gast, C.J., 2014. Long-term changes in soil microbial communities during primary succession. Soil Biology & Biochemistry69, 359–370.

19 de Vries, F.T., Manning, P., Tallowin, J.R.B., Mortimer, S.R., Pilgrim, E.S., Harrison, K.A., Hobbs, P.J., Quirk, H., Shipley, B., Cornelissen, J.H.C., Kattge, J., Bardgett, R.D., 2012. Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecology Letters15, 1230–1239.

20 de Vries, F.T., Thion, C., Bahn, M., Bergk Pinto, B., Cécillon, S., Frey, B., Grant, H., Nicol, G.W., Wanek, W., Prosser, J.I., Bardgett, R.D., 2021. Glacier forelands reveal fundamental plant and microbial controls on short-term ecosystem nitrogen retention. Journal of Ecology109, 3710–3723.

21 Deiglmayr, K., Philippot, L., Tscherko, D., Kandeler, E., 2006. Microbial succession of nitrate-reducing bacteria in the rhizosphere of Poa alpina across a glacier foreland in the Central Alps. Environmental Microbiology8, 1600–1612.

22 Delgado-Baquerizo, M., Bardgett, R.D., Vitousek, P.M., Maestre, F.T., Williams, M.A., Eldridge, D.J., Lambers, H., Neuhauser, S., Gallardo, A., García-Velázquez, L., Sala, O.E., Abades, S.R., Alfaro, F.D., Berhe, A.A., Bowker, M.A., Currier, C.M., Cutler, N.A., Hart, S.C., Hayes, P.E., Hseu, Z.Y., Kirchmair, M., Peña-Ramírez, V.M., Pérez, C.A., Reed, S.C., Santos, F., Siebe, C., Sullivan, B.W., Weber-Grullon, L., Fierer, N., 2019. Changes in belowground biodiversity during ecosystem development. Proceedings of the National Academy of Sciences of the United States of America116, 6891–6896.

23 Dequiedt, S., Saby, N.P.A., Lelievre, M., Jolivet, C., Thioulouse, J., Toutain, B., Arrouays, D., Bispo, A., Lemanceau, P., Ranjard, L., 2011. Biogeographical patterns of soil molecular microbial biomass as influenced by soil characteristics and management. Global Ecology and Biogeography20, 641–652.

24 Dimitriu, P.A., Grayston, S.J., 2010. Relationship between soil properties and patterns of bacterial beta-diversity across reclaimed and natural boreal forest soils. Microbial Ecology59, 563–573.

25 Dini-Andreote, F., de Cássia Pereira e Silva, M., Triadó-Margarit, X., Casamayor, E.O., van Elsas, J.D., Salles, J.F., 2014. Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning. ISME Journal8, 1989–2001.

26 Dini-Andreote, F., Stegen, J.C., van Elsas, J.D., Salles, J.F., 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proceedings of the National Academy of Sciences of the United States of America112, E1326–E1332.

27 Dong, K., Yu, Z., Kerfahi, D., Lee, S., Li, N., Yang, T., Adams, J.M., 2022. Soil microbial co-occurrence networks become less connected with soil development in a high Arctic glacier foreland succession. Science of the Total Environment813, 152565.

28 Edwards, I.P., Burgmann, H., Miniaci, C., Zeyer, J., 2006. Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina (L. ) Heywood and adjacent bare soil along an alpine chronosequence. Microbial Ecology52, 679–692.

29 Faust, K., Sathirapongsasuti, J.F., Izard, J., Segata, N., Gevers, D., Raes, J., Huttenhower, C., 2012. Microbial co-occurrence relationships in the human microbiome. PLoS Computational Biology8, e1002606.

30 Ferrenberg, S., O’Neill, S.P., Knelman, J.E., Todd, B., Duggan, S., Bradley, D., Robinson, T., Schmidt, S.K., Townsend, A.R., Williams, M.W., Cleveland, C.C., Melbourne, B.A., Jiang, L., Nemergut, D.R., 2013. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME Journal7, 1102–1111.

31 Fierer, N., Jackson, J.A., Vilgalys, R., Jackson, R.B., 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology71, 4117–4120.

32 Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America103, 626–631.

33 Freedman, Z., Zak, D.R., 2015. Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long-term chronosequence. Environmental Microbiology17, 3208–3218.

34 Freeman, K.R., Pescador, M.Y., Reed, S.C., Costello, E.K., Robeson, M.S., Schmidt, S.K., 2009. Soil CO₂ flux and photoautotrophic community composition in high-elevation, ‘barren’ soil. Environmental Microbiology11, 674–686.

35 Harper, K.T., Belnap, J., 2001. The influence of biological soil crusts on mineral uptake by associated vascular plants. Journal of Arid Environments47, 347–357.

36 He, L., Tang, Y., 2008. Soil development along primary succession sequences on moraines of Hailuogou Glacier, Gongga Mountain, Sichuan, China. Catena72, 259–269.

37 Hodkinson, I.D., Coulson, S.J., Webb, N.R., 2003. Community assembly along proglacial chronosequences in the high Arctic: vegetation and soil development in north-west Svalbard. Journal of Ecology91, 651–663.

38 Ives, A.R., Dennis, B., Cottingham, K.L., Carpenter, S.R., 2003. Estimating community stability and ecological interactions from time-series data. Ecological Monographs73, 301–330.

39 Jackson, C.R., Churchill, P.F., Roden, E.E., 2001. Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology82, 555–566.

40 Janatkova, K., Rehakova, K., Dolezal, J., Šimek, M., Chlumská, Z., Dvorský, M., Kopecký, M., 2013. Community structure of soil phototrophs along environmental gradients in arid Himalaya. Environmental Microbiology15, 2505–2516.

41 Jangid, K., Whitman, W.B., Condron, L.M., Turner, B.L., Williams, M.A., 2013. Soil bacterial community succession during long-term ecosystem development. Molecular Ecology22, 3415–3424.

42 Jiao, S., Lu, Y., Wei, G., 2022. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Global Change Biology28, 140–153.

43 Jones, R.T., Robeson, M.S., Lauber, C.L., Hamady, M., Knight, R., Fierer, N., 2009. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME Journal3, 442–453.

44 Jumpponen, A., Brown, S.P., Trappe, J.M., Cázares, E., Strömmer, R., 2012. Twenty years of research on fungal–plant interactions on Lyman Glacier forefront – lessons learned and questions yet unanswered. Fungal Ecology5, 430–442.

45 Jun, W., Barahona, M., Yue-jin, T., Hong-Zhong, D., 2010. Natural connectivity of complex networks. Chinese Physics Letters27, 078902.

46 Kerfahi, D., Tateno, R., Takahashi, K., Cho, H.J., Kim, H., Adams, J.M., 2017. Development of soil bacterial communities in volcanic ash microcosms in a range of climates. Microbial Ecology73, 775–790.

47 Kim, M., Jung, J.Y., Laffly, D., Kwon, H.Y., Lee, Y.K., 2017. Shifts in bacterial community structure during succession in a glacier foreland of the High Arctic. FEMS Microbiology Ecology93, fiw213.

48 Lamb, E.G., Han, S., Lanoil, B.D., Henry, G.H.R., Brummell, M., Banerjee, S., Siciliano, S.D., 2011. A High Arctic soil ecosystem resists long-term environmental manipulations. Global Change Biology17, 3187–3194.

49 Lauber, C.L., Hamady, M., Knight, R., Fierer, N., 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology75, 5111–5120.

50 Lauber, C.L., Ramirez, K.S., Aanderud, Z., Lennon, J., Fierer, N., 2013. Temporal variability in soil microbial communities across land-use types. ISME Journal7, 1641–1650.

51 Ling, N., Zhu, C., Xue, C., Chen, H., Duan, Y., Peng, C., Guo, S., Shen, Q., 2016. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biology & Biochemistry99, 137–149.

52 Ma, B., Wang, H., Dsouza, M., Lou, J., He, Y., Dai, Z., Brookes, P.C., Xu, J., Gilbert, J.A., 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME Journal10, 1891–1901.

53 Mapelli, F., Marasco, R., Fusi, M., Scaglia, B., Tsiamis, G., Rolli, E., Fodelianakis, S., Bourtzis, K., Ventura, S., Tambone, F., Adani, F., Borin, S., Daffonchio, D., 2018. The stage of soil development modulates rhizosphere effect along a High Arctic desert chronosequence. ISME Journal12, 1188–1198.

54 Moritz, R.E., Bitz, C.M., Steig, E.J., 2002. Dynamics of recent climate change in the Arctic. Science297, 1497–1502.

55 Nakayama, M., Imamura, S., Taniguchi, T., Tateno, R., 2019. Does conversion from natural forest to plantation affect fungal and bacterial biodiversity, community structure, and co-occurrence networks in the organic horizon and mineral soil? Forest Ecology and Management 446, 238–250

56 Nemergut, D.R., Anderson, S.P., Cleveland, C.C., Martin, A.P., Miller, A.E., Seimon, A., Schmidt, S.K., 2007. Microbial community succession in an unvegetated, recently deglaciated soil. Microbial Ecology53, 110–122.

57 Newman, M.E.J., 2006. Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America103, 8577–8582.

58 Ning, D., Yuan, M., Wu, L., Zhang, Y., Guo, X., Zhou, X., Yang, Y., Arkin, A.P., Firestone, M.K., Zhou, J., 2020. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nature Communications11, 4717.

59 Ochoa-Hueso, R., Eldridge, D.J., Delgado‐Baquerizo, M., Soliveres, S., Bowker, M.A., Gross, N., Le Bagousse-Pinguet, Y., Quero, J.L., García-Gómez, M., Valencia, E., Arredondo, T., Beinticinco, L., Bran, D., Cea, A., Coaguila, D., Dougill, A.J., Espinosa, C.I., Gaitán, J., Guuroh, R.T., Guzman, E., Gutiérrez, J.R., Hernández, R.M., Huber-Sannwald, E., Jeffries, T., Linstädter, A., Mau, R.L., Monerris, J., Prina, A., Pucheta, E., Stavi, I., Thomas, A.D., Zaady, E., Singh, B.K., Maestre, F.T., 2017. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. Journal of Ecology106, 242–253.

60 Odum, E.P., 1969. The strategy of ecosystem development. Science164, 262–270.

61 Osburn, E.D., Aylward, F.O., Barrett, J.E., 2021. Historical land use has long-term effects on microbial community assembly processes in forest soils. ISME Communications1, 48.

62 Paerl, H.W., Gallucci, K.K., 1985. Role of chemotaxis in establishing a specific nitrogen-fixing cyanobacterial-bacterial association. Science227, 647–649.

63 Perera, I., Subashchandrabose, S.R., Venkateswarlu, K., Naidu, R., Megharaj, M., 2018. Consortia of cyanobacteria/microalgae and bacteria in desert soils: an underexplored microbiota. Applied Microbiology and Biotechnology102, 7351–7363.

64 Philippot, L., Andersson, S.G., Battin, T.J., Prosser, J.I., Schimel, J.P., Whitman, W.B., Hallin, S., 2010. The ecological coherence of high bacterial taxonomic ranks. Nature Reviews Microbiology8, 523–529.

65 Pombubpa, N., Pietrasiak, N., De Ley, P., Stajich, J.E., 2020. Insights into dryland biocrust microbiome: geography, soil depth and crust type affect biocrust microbial communities and networks in Mojave Desert, USA. FEMS Microbiology Ecology96, 96.

66 Poosakkannu, A., Nissinen, R., Mannisto, M., Kytöviita, M.M., 2017. Microbial community composition but not diversity changes along succession in arctic sand dunes. Environmental Microbiology19, 698–709.

67 Price, M.N., Dehal, P.S., Arkin, A.P., 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Molecular Biology and Evolution26, 1641–1650.

68 Rime, T., Hartmann, M., Brunner, I., Widmer, F., Zeyer, J., Frey, B., 2015. Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Molecular Ecology24, 1091–1108.

69 Rousk, J., Baath, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal4, 1340–1351.

70 Ruan, Q., Dutta, D., Schwalbach, M.S., Steele, J.A., Fuhrman, J.A., Sun, F., 2006. Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics (Oxford, England)22, 2532–2538.

71 Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., Weber, C.F., 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology75, 7537–7541.

72 Schutte, U.M., Abdo, Z., Bent, S.J., Williams, C.J., Schneider, G.M., Solheim, B., Forney, L.J., 2009. Bacterial succession in a glacier foreland of the High Arctic. ISME Journal3, 1258–1268.

73 Sigler, W.V., Crivii, S., Zeyer, J., 2002. Bacterial succession in glacial forefield soils characterized by community structure, activity and opportunistic growth dynamics. Microbial Ecology44, 306–316.

74 Sigler, W.V., Zeyer, J., 2002. Microbial diversity and activity along the forefields of two receding glaciers. Microbial Ecology43, 397–407.

75 Tripathi, B.M., Stegen, J.C., Kim, M., Dong, K., Adams, J.M., Lee, Y.K., 2018. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME Journal12, 1072–1083.

76 Tscherko, D., Hammesfahr, U., Marx, M.C., Kandeler, E., 2004. Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biology & Biochemistry36, 1685–1698.

77 Walker, L.R., del Moral, R., 2010. Primary Succession and Ecosystem Rehabilitation. Cambridge University Press, Cambridge.

78 Williams, M.A., Jangid, K., Shanmugam, S.G., Whitman, W.B., 2013. Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons. Soil Biology & Biochemistry57, 749–757.

79 Wu, M., Chen, S., Chen, J., Xue, K., Chen, S.L., Wang, X.M., Chen, T., Kang, S.C., Rui, J.P., Thies, J.E., Bardgett, R.D., Wang, Y.F., 2021. Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation. Proceedings of the National Academy of Sciences of the United States of America118, 25.

80 Xue, L., Ren, H., Brodribb, T.J., Wang, J., Yao, X., Li, S., 2020. Long term effects of management practice intensification on soil microbial community structure and co-occurrence network in a non-timber plantation. Forest Ecology and Management459, 459.

81 Yang, T., Tedersoo, L., Liu, X., Gao, G.F., Dong, K., Adams, J.M., Chu, H., 2022. Fungi stabilize multi-kingdom community in a high elevation timberline ecosystem. iMeta1, 4–e49.

82 Yang, Y., Shi, Y., Kerfahi, D., Ogwu, M.C., Wang, J., Dong, K., Takahashi, K., Moroenyane, I., Adams, J.M., 2021. Elevation-related climate trends dominate fungal co-occurrence network structure and the abundance of keystone taxa on Mt. Norikura, Japan. Science of the Total Environment799, 149368.

83 Yeager, C.M., Kornosky, J.L., Housman, D.C., Grote, E.E., Belnap, J., Kuske, C.R., 2004. Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Applied and Environmental Microbiology70, 973–983.

84 Zumsteg, A., Bernasconi, S.M., Zeyer, J., Frey, B., 2011. Microbial community and activity shifts after soil transplantation in a glacier forefield. Applied Geochemistry26, S326–S9.