Reproducible Propagation of Species-Rich Soil Microbiomes Suggests Robust Underlying Deterministic Principles of Community Formation

Microbiomes are typically characterised by high species diversity but it is poorly understood how such system-level complexity can be generated and propagated. Here, we used soils as a relevant model to study microbiome development. Despite inherent stochastic variation in manipulating species-rich communities, both laboratory-mixed medium complexity (21 soil bacterial isolates in equal proportions) and high-diversity natural top-soil communities followed highly reproducible succession paths, maintaining distinct soil microbiome signatures. Development trajectories and compositional states were different for communities propagated in soils than in liquid suspension. Microbiome states were maintained over multiple renewed growth cycles but could be diverged by short-term pollutant exposure. The different but robust trajectories demonstrated that deterministic taxa-inherent characteristics underlie reproducible development and self-organized complexity of soil microbiomes within their environmental boundary conditions. Our findings also have direct implications for potential strategies to achieve controlled restoration of desertified land. TEASER Species-rich soil microbiomes grow and propagate reproducibly despite inherent stochastic complexity, paving the way for soil restoration.

[1]  Michael L. Waskom,et al.  Seaborn: Statistical Data Visualization , 2021, J. Open Source Softw..

[2]  Colin J. Brislawn,et al.  Deconstructing the Soil Microbiome into Reduced-Complexity Functional Modules , 2020, mBio.

[3]  Otto X. Cordero,et al.  Context-dependent dynamics lead to the assembly of functionally distinct microbial communities , 2020, Nature Communications.

[4]  D. J. Kiviet,et al.  Short-range interactions govern the dynamics and functions of microbial communities , 2019, Nature Ecology & Evolution.

[5]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[6]  S. Retterer,et al.  Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales , 2019, Applied and Environmental Microbiology.

[7]  Lai Guan Ng,et al.  Dimensionality reduction for visualizing single-cell data using UMAP , 2018, Nature Biotechnology.

[8]  Alexander Loy,et al.  Stable-Isotope Probing of Human and Animal Microbiome Function , 2018, Trends in microbiology.

[9]  Falk Hildebrand,et al.  Structure and function of the global topsoil microbiome , 2018, Nature.

[10]  Fan Yang,et al.  Greatest soil microbial diversity found in micro-habitats , 2018 .

[11]  E. Shakhnovich,et al.  Growth tradeoffs produce complex microbial communities on a single limiting resource , 2018, bioRxiv.

[12]  D. Or,et al.  Hydration status and diurnal trophic interactions shape microbial community function in desert biocrusts , 2017 .

[13]  G. Mishra Microbes in Heavy Metal Remediation: A Review on Current Trends and Patents. , 2017, Recent patents on biotechnology.

[14]  Rick L. Stevens,et al.  A communal catalogue reveals Earth’s multiscale microbial diversity , 2017, Nature.

[15]  Mikhail Tikhonov,et al.  Emergent simplicity in microbial community assembly , 2017, Science.

[16]  N. Fierer Embracing the unknown: disentangling the complexities of the soil microbiome , 2017, Nature Reviews Microbiology.

[17]  Christian von Mering,et al.  MAPseq: highly efficient k-mer search with confidence estimates, for rRNA sequence analysis , 2017, Bioinform..

[18]  G. Rzepa,et al.  Soil formation and initial microbiological activity on a foreland of an Arctic glacier (SW Svalbard) , 2017 .

[19]  David R. Johnson,et al.  Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations , 2017, The ISME Journal.

[20]  R. Kolter,et al.  Simplified and representative bacterial community of maize roots , 2017, Proceedings of the National Academy of Sciences.

[21]  W. H. van der Putten,et al.  Low abundant soil bacteria can be metabolically versatile and fast growing. , 2017, Ecology.

[22]  Jeff Gore,et al.  Community structure follows simple assembly rules in microbial microcosms , 2016, Nature Ecology &Evolution.

[23]  Daniel B. Müller,et al.  The Plant Microbiota: Systems-Level Insights and Perspectives. , 2016, Annual review of genetics.

[24]  Jeff Gore,et al.  Resource Availability Modulates the Cooperative and Competitive Nature of a Microbial Cross-Feeding Mutualism , 2016, PLoS biology.

[25]  Otto X. Cordero,et al.  Microbial interactions and community assembly at microscales. , 2016, Current opinion in microbiology.

[26]  Se Jin Song,et al.  The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions , 2016, mBio.

[27]  Orkun S. Soyer,et al.  Challenges in microbial ecology: building predictive understanding of community function and dynamics , 2016, The ISME Journal.

[28]  Elin E. Lilja,et al.  Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates , 2016, The ISME Journal.

[29]  Mary Ann Moran,et al.  The global ocean microbiome , 2015, Science.

[30]  P. Silver,et al.  Better together: engineering and application of microbial symbioses. , 2015, Current opinion in biotechnology.

[31]  D. Sparks,et al.  Soil and human security in the 21st century , 2015, Science.

[32]  Alan Edelman,et al.  Julia: A Fresh Approach to Numerical Computing , 2014, SIAM Rev..

[33]  Jeff Gore,et al.  Clustering in community structure across replicate ecosystems following a long-term bacterial evolution experiment , 2014, Nature Communications.

[34]  Jo Handelsman,et al.  Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity , 2014, mBio.

[35]  James J Collins,et al.  Syntrophic exchange in synthetic microbial communities , 2014, Proceedings of the National Academy of Sciences.

[36]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[37]  X. Raynaud,et al.  Spatial Ecology of Bacteria at the Microscale in Soil , 2014, PloS one.

[38]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[39]  Elmar Pruesse,et al.  SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes , 2012, Bioinform..

[40]  N. Ono,et al.  Cooperative Adaptation to Establishment of a Synthetic Bacterial Mutualism , 2011, PloS one.

[41]  P. Silver,et al.  Dynamics in the mixed microbial concourse. , 2010, Genes & development.

[42]  Juan Liu,et al.  An improved method for extracting bacteria from soil for high molecular weight DNA recovery and BAC library construction , 2010, The Journal of Microbiology.

[43]  R. Spencer,et al.  Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: A review , 2010 .

[44]  A. Mrozik,et al.  Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. , 2010, Microbiological research.

[45]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[46]  J. Choi,et al.  Defined spatial structure stabilizes a synthetic multispecies bacterial community , 2008, Proceedings of the National Academy of Sciences.

[47]  M. V. D. van der Heijden,et al.  The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. , 2008, Ecology letters.

[48]  Hadley Wickham,et al.  Reshaping Data with the reshape Package , 2007 .

[49]  S. Reed,et al.  Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. , 2007, Ecology.

[50]  Susan M. Huse,et al.  Microbial diversity in the deep sea and the underexplored “rare biosphere” , 2006, Proceedings of the National Academy of Sciences.

[51]  J. Megonigal,et al.  SEASONAL PATTERNS AND PLANT‐MEDIATED CONTROLS OF SUBSURFACE WETLAND BIOGEOCHEMISTRY , 2005 .

[52]  J. Prosser,et al.  Primary succession of soil Crenarchaeota across a receding glacier foreland. , 2005, Environmental microbiology.

[53]  Jocelyn Kaiser,et al.  Wounding Earth's Fragile Skin , 2004, Science.

[54]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[55]  A. Magurran,et al.  Explaining the excess of rare species in natural species abundance distributions , 2003, Nature.

[56]  T. Vogel Bioaugmentation as a soil bioremediation approach. , 1996, Current opinion in biotechnology.

[57]  P. Pritchard Use of inoculation in bioremediation , 1992 .

[58]  N. Pace,et al.  Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[59]  D. Balkwill,et al.  Characterization of Subsurface Bacteria Associated with Two Shallow Aquifers in Oklahoma , 1985, Applied and environmental microbiology.

[60]  C. S. Holling Resilience and Stability of Ecological Systems , 1973 .