Modifying and reacting to the environmental pH can drive bacterial interactions

Microbes usually exist in communities consisting of myriad different but interacting species. These interactions are typically mediated through environmental modifications; microbes change the environment by taking up resources and excreting metabolites, which affects the growth of both themselves and also other microbes. We show here that the way microbes modify their environment and react to it sets the interactions within single-species populations and also between different species. A very common environmental modification is a change of the environmental pH. We find experimentally that these pH changes create feedback loops that can determine the fate of bacterial populations; they can either facilitate or inhibit growth, and in extreme cases will cause extinction of the bacterial population. Understanding how single species change the pH and react to these changes allowed us to estimate their pairwise interaction outcomes. Those interactions lead to a set of generic interaction motifs—bistability, successive growth, extended suicide, and stabilization—that may be independent of which environmental parameter is modified and thus may reoccur in different microbial systems.

[1]  F. Bazzaz The Physiological Ecology of Plant Succession , 1979 .

[2]  J. Gore,et al.  Ecological suicide in microbes , 2017, Nature Ecology & Evolution.

[3]  J. Costerton,et al.  Interspecies bacterial interactions in biofilms , 1995, Journal of Industrial Microbiology.

[4]  P. Brookes,et al.  Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization , 2009, Applied and Environmental Microbiology.

[5]  R. Knight,et al.  A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses , 2009, The ISME Journal.

[6]  Wenying Shou,et al.  Synthetic cooperation in engineered yeast populations , 2007, Proceedings of the National Academy of Sciences.

[7]  Peter Rashkov,et al.  Stability of Cross-Feeding Polymorphisms in Microbial Communities , 2016, PLoS Comput. Biol..

[8]  N. Rius,et al.  Rapid extracellular acidification induced by glucose metabolism in non-proliferating cells of Serratia marcescens. , 2000, International microbiology : the official journal of the Spanish Society for Microbiology.

[9]  V. Scheffer,et al.  The Rise and Fall of a Reindeer Herd , 1951 .

[10]  L. T. Angenent,et al.  Succession of microbial consortia in the developing infant gut microbiome , 2010, Proceedings of the National Academy of Sciences.

[11]  N. C. Mehta,et al.  Carbohydrates in the soil. , 1961, Advances in carbohydrate chemistry.

[12]  H. Šantrůčková,et al.  Direct determination of total soil carbohydrate content , 1992, Plant and Soil.

[13]  Jeff Gore,et al.  Oscillatory dynamics in a bacterial cross-protection mutualism , 2016, Proceedings of the National Academy of Sciences.

[14]  L. McCook,et al.  Understanding ecological community succession: Causal models and theories, a review , 2004, Vegetatio.

[15]  Sara Mitri,et al.  The Ecology and Evolution of Microbial Competition. , 2016, Trends in microbiology.

[16]  M. Hindell Some life-history parameters of a declining population of southern elephant seals, Mirounga leonina , 1991 .

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

[18]  C. Schleper,et al.  The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. , 2008, Environmental microbiology.

[19]  M. Riley,et al.  The ecological role of bacteriocins in bacterial competition. , 1999, Trends in microbiology.

[20]  J. Russell,et al.  Factors That Alter Rumen Microbial Ecology , 2001, Science.

[21]  William J. Sutherland,et al.  What Is the Allee Effect , 1999 .

[22]  Harry J Flint,et al.  Interactions and competition within the microbial community of the human colon: links between diet and health. , 2007, Environmental microbiology.

[23]  M. Collins Transfer of Brevibacterium ammoniagenes (Cooke and Keith) to the Genus Corynebacterium as Corynebacterium ammoniagenes comb. nov. , 1987 .

[24]  Stefan Schuster,et al.  Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria , 2013, The ISME Journal.

[25]  C. Fuqua,et al.  Bacterial competition: surviving and thriving in the microbial jungle , 2010, Nature Reviews Microbiology.

[26]  Marten Scheffer,et al.  Tipping elements in the human intestinal ecosystem , 2014, Nature Communications.

[27]  R. Quivey,et al.  Adaptation of oral streptococci to low pH. , 2000, Advances in microbial physiology.

[28]  E. Percival Advances in Carbohydrate Chemistry , 1947, Nature.

[29]  A. P. Mathews,et al.  Lactic acid production from lactose by Lactobacillus plantarum: kinetic model and effects of pH, substrate, and oxygen , 1999 .

[30]  Jonathan Friedman,et al.  Co-occurring soil bacteria exhibit a robust competitive hierarchy and lack of non-transitive interactions , 2017, bioRxiv.

[31]  B. Ma,et al.  Soil bulk density effects on soil microbial populations and enzyme activities during the growth of maize (Zea mays L.) planted in large pots under field exposure , 2002 .

[32]  M. Muir Physical Chemistry , 1888, Nature.

[33]  R. Gudi,et al.  pH of Drinking Water Influences the Composition of Gut Microbiome and Type 1 Diabetes Incidence , 2014, Diabetes.

[34]  I. Brook Inoculum effect. , 1989, Reviews of infectious diseases.

[35]  J. Gore,et al.  Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population , 2016, Nature Microbiology.

[36]  D. Klein The introduction, increase, and crash of reindeer on St. Matthew Island. , 1968 .

[37]  M. Feldman,et al.  Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors , 2002, Nature.

[38]  P. Bork,et al.  Molecular eco-systems biology: towards an understanding of community function , 2008, Nature Reviews Microbiology.

[39]  J. Fuhrman General Distributions and the 'rare Biosphere' Microbial Community Structure and Its Functional Implications Review Insight , 2022 .

[40]  G. C. L. Bertram,et al.  Principles of animal ecology , 1951 .

[41]  I. R. Hamilton,et al.  Environmental pH as a factor in the competition between strains of the oral streptococci Streptococcus mutans, S. sanguis, and "S. mitior" growing in continuous culture. , 1987, Canadian journal of microbiology.

[42]  R. Rosenzweig,et al.  Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. , 1994, Genetics.

[43]  A. van Oudenaarden,et al.  Snowdrift game dynamics and facultative cheating in yeast , 2009, Nature.

[44]  Otto X. Cordero,et al.  Microbial interactions lead to rapid micro-scale successions on model marine particles , 2016, Nature Communications.

[45]  M. Sung,et al.  A novel microbial interaction: obligate commensalism between a new gram-negative thermophile and a thermophilic Bacillus strain , 2000, Extremophiles.

[46]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[47]  V. Nurmikko Biochemical factors affecting symbiosis among bacteria , 1956, Experientia.

[48]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[49]  Jeff Gore,et al.  Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids , 2013, Molecular systems biology.

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

[51]  Grenfell,et al.  Inverse density dependence and the Allee effect. , 1999, Trends in ecology & evolution.

[52]  J. Russell,et al.  Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture , 1980, Applied and environmental microbiology.

[53]  C. Kost,et al.  Bacterial Unculturability and the Formation of Intercellular Metabolic Networks. , 2017, Trends in microbiology.

[54]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Strom Microbial Ecology of Ocean Biogeochemistry: A Community Perspective , 2008, Science.

[56]  A. Aertsen,et al.  Bacterial interactions in biofilms , 2009, Critical reviews in microbiology.

[57]  J. Raes,et al.  Microbial interactions: from networks to models , 2012, Nature Reviews Microbiology.

[58]  M. Riley,et al.  Bacteriocins: evolution, ecology, and application. , 2002, Annual review of microbiology.

[59]  H. Stone,et al.  Solutions to the Public Goods Dilemma in Bacterial Biofilms , 2013, Current Biology.

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

[61]  Lee Alan Dugatkin,et al.  Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm , 2005, Proceedings of the Royal Society B: Biological Sciences.

[62]  Barbara Mayer,et al.  Microbial Ecology Fundamentals And Applications , 2016 .

[63]  J. Gore,et al.  Cellular cooperation: insights from microbes. , 2013, Trends in cell biology.

[64]  S. Pocock,et al.  Incidence , , 2018 .