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Title: Conditional filamentation as an adaptive trait of bacteria and its ecological significance in soils

Journal Article · · Environmental Microbiology

Summary Bacteria can regulate cell morphology in response to environmental conditions, altering their physiological and metabolic characteristics to improve survival. Conditional filamentation, in which cells suspend division while continuing lateral growth, is a strategy with a range of adaptive benefits. Here, we review the causes and consequences of conditional filamentation with respect to bacterial physiology, ecology and evolution. We describe four major benefits from conditional filamentation: stress tolerance, surface colonization, gradient spanning and the facilitation of biotic interactions. Adopting a filamentous growth habit involves fitness trade‐offs which are also examined. We focus on the role of conditional filamentation in soil habitats, where filamentous morphotypes are highly prevalent and where environmental heterogeneity can benefit a conditional response. To illustrate the use of information presented in our review, we tested the conditions regulating filamentation by the forest soil isolate Paraburkholderia elongata 5N T . Filamentation by P. elongata was induced at elevated phosphate concentrations, and was associated with the accumulation of intracellular polyphosphate, highlighting the role of filamentation in a phosphate‐solubilizing bacterium. Conditional filamentation enables bacteria to optimize their growth and metabolism in environments that are highly variable, a trait that can impact succession, symbioses, and biogeochemistry in soil environments.

Research Organization:
Cornell Univ., Ithaca, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0016364; DE‐SC0016364
OSTI ID:
1863903
Alternate ID(s):
OSTI ID: 1897334
Journal Information:
Environmental Microbiology, Vol. 24, Issue 1; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (160)

Streptomyces exploration is triggered by fungal interactions and volatile signals journal January 2017
Isolation and characterization of Rhizobium sp. strain YS-1r that degrades lignin in plant biomass journal February 2017
Magnesium-induced Linear Self-association of the FtsZ Bacterial Cell Division Protein Monomer journal April 2000
Induced sensitivity of Bacillus subtilis colony morphology to mechanical media compression journal January 2014
Staying in Shape: the Impact of Cell Shape on Bacterial Survival in Diverse Environments journal February 2016
Thermotolerance, cell filamentation, and induced protein synthesis in psychrophilic and psychrotrophic bacteria journal May 1990
Long-Chain Polyphosphate Causes Cell Lysis and Inhibits Bacillus cereus Septum Formation, Which Is Dependent on Divalent Cations journal September 1999
Biochemical Basis for Whole-Cell Uptake Kinetics: Specific Affinity, Oligotrophic Capacity, and the Meaning of the Michaelis Constant journal January 1991
A Rhizobiales-Specific Unipolar Polysaccharide Adhesin Contributes to Rhodopseudomonas palustris Biofilm Formation across Diverse Photoheterotrophic Conditions journal December 2016
Oxygen Concentration and Redox Potential Gradients in Unsaturated Model Soil Aggregates journal January 1993
Effects of Inorganic Polyphosphate on the Proteolytic and DNA-binding Activities of Lon in Escherichia coli journal August 2004
β-Lactams and β-Lactamase Inhibitors: An Overview journal June 2016
Cell division, guillotining of dimer chromosomes and SOS induction in resolution mutants (dif, xerC and xerD) of Escherichia coli journal May 2000
Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential journal January 2011
A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW journal June 2011
Pathways of nitrogen utilization by soil microorganisms – A review journal December 2010
The Role of L-Glutamine in the Phenotypic Change of a rod Mutant Derived from Bacillus subtilis 168 journal May 1970
Impact of Small-Scaled Differences in Micro-Aggregation on Physico-Chemical Parameters of Macroscopic Biopore Walls journal August 2018
Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells journal April 1993
Genetic Analysis of Functions Involved in Adhesion of Pseudomonas putida to Seeds journal January 2000
Reduced Water Availability Influences the Dynamics, Development, and Ultrastructural Properties of Pseudomonas putida Biofilms journal October 2003
Cable bacteria reduce methane emissions from rice-vegetated soils journal April 2020
The Potato Yam Phyllosphere Ectosymbiont Paraburkholderia sp. Msb3 Is a Potent Growth Promotor in Tomato journal April 2020
Microfluidic growth chambers with optical tweezers for full spatial single-cell control and analysis of evolving microbes journal December 2013
Polyfunctional Nanofibril Appendages Mediate Attachment, Filamentation, and Filament Adaptability in Leptothrix cholodnii journal December 2019
Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. journal January 2002
Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria journal June 2020
Build your own soil: exploring microfluidics to create microbial habitat structures journal November 2017
Chirality provides a direct fitness advantage and facilitates intermixing in cellular aggregates journal December 2018
Formation of Filaments by Pseudomonas putida journal August 1985
Glutamine-induced filamentous cells of Pseudomonas mediterranea CFBP-5447T as producers of PHAs journal October 2019
Microbial Community Structure and Dynamics in the Largest Natural French Lake (Lake Bourget) journal May 2006
Molecular Basis and Ecological Relevance of Caulobacter Cell Filamentation in Freshwater Habitats journal August 2019
A trap for in situ cultivation of filamentous actinobacteria journal March 2008
Cell Division Defects in Escherichia coli Deficient in the Multidrug Efflux Transporter AcrEF-TolC journal November 2005
Inorganic Polyphosphate: Essential for Growth and Survival journal June 2009
Labile carbon supplement induces growth of filamentous bacteria in the Baltic Sea journal May 2012
Mutations in Escherichia coli Polyphosphate Kinase That Lead to Dramatically Increased In Vivo Polyphosphate Levels journal January 2018
In Silico Characterization and Phylogenetic Distribution of Extracellular Matrix Components in the Model Rhizobacteria Pseudomonas fluorescens F113 and Other Pseudomonads journal November 2020
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Functioning of cyanobacteria in soil ecosystems journal December 2006
Filament formation by foodborne bacteria under sublethal stress journal July 2013
Succession of cable bacteria and electric currents in marine sediment journal January 2014
Role of Inorganic Polyphosphate in Promoting Ribosomal Protein Degradation by the Lon Protease in E. coli journal July 2001
The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level journal December 2007
Fine-Tuning of the Cpx Envelope Stress Response Is Required for Cell Wall Homeostasis in Escherichia coli journal February 2016
Gene product 0.4 increases bacteriophage T7 competitiveness by inhibiting host cell division journal November 2013
Microbial Extracellular Polymeric Substances: Ecological Function and Impact on Soil Aggregation journal July 2018
Image-Based Dynamic Phenotyping Reveals Genetic Determinants of Filamentation-Mediated β-Lactam Tolerance journal March 2020
Phosphate-starvation induced changes in Thiobacillus ferrooxidans journal March 1993
Diversity Takes Shape: Understanding the Mechanistic and Adaptive Basis of Bacterial Morphology journal October 2016
Soil-on-a-Chip: microfluidic platforms for environmental organismal studies journal January 2016
A Biosensor-Based Assay ( GlnLux -Agar) Shows Defoliation Triggers Rapid Release of Glutamine from Nodules and Young Roots of Forage Legumes journal January 2019
Unique inducible filamentous motility identified in pathogenic Bacillus cereus group species journal August 2020
An isolated cellulolytic Escherichia coli from bovine rumen produces ethanol and hydrogen from corn straw journal June 2017
Bacillus amyloliquefaciens Spore Production Under Solid-State Fermentation of Lignocellulosic Residues journal December 2017
Ecophysiological Study of Paraburkholderia sp. Strain 1N under Soil Solution Conditions: Dynamic Substrate Preferences and Characterization of Carbon Use Efficiency journal November 2020
The role of glutamine synthetase in regulation of nitrogen metabolism within the soil microbial community journal March 1995
Long-distance electron transfer by cable bacteria in aquifer sediments journal April 2016
Bloom of Filamentous Bacteria in a Mesotrophic Lake: Identity and Potential Controlling Mechanism journal October 2004
Paraburkholderia phosphatilytica sp. nov., a phosphate-solubilizing bacterium isolated from forest soil journal January 2019
Polyphosphate granule biogenesis is temporally and functionally tied to cell cycle exit during starvation in Pseudomonas aeruginosa journal March 2017
Formation of Filaments and Synthesis of Macromolecules at Temperatures Below the Minimum for Growth of Escherichia coli journal January 1968
Effect of cellular filamentation on adventurous and social gliding motility of Myxococcus xanthus journal December 1999
Long-term effects of timber harvesting on hemicellulolytic microbial populations in coniferous forest soils journal August 2015
Disruption of lipid homeostasis in the Gram-negative cell envelope activates a novel cell death pathway journal February 2016
Filamentous Cells of Escherichia coli Formed in the Presence of Mitomycin journal February 1967
The SOS regulatory system of Escherichia coli journal May 1982
Bacterial Filament Formation, a Defense Mechanism against Flagellate Grazing, Is Growth Rate Controlled in Bacteria of Different Phyla journal January 1999
Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil journal February 2021
Big Bacteria journal October 2001
Some aspects of the SOS response system--a critical survey. journal September 2001
Contribution of Cell Elongation to the Biofilm Formation of Pseudomonas aeruginosa during Anaerobic Respiration journal January 2011
Proximity of Agrobacterium to living plant tissues induces conversion to a filamentous bacterial form journal February 2001
The Race to the Pole: How High-Aspect Ratio Shape and Heterogeneous Environments Limit Phagocytosis of Filamentous Escherichia coli Bacteria by Macrophages journal May 2012
A cell length-dependent transition in MinD-dynamics promotes a switch in division-site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells journal August 2018
Breakdown of Douglas-fir phloem by a lignocellulose-degradingStreptomyces journal March 1979
Structural Basis for the Magnesium-Dependent Activation and Hexamerization of the Lon AAA+ Protease journal May 2016
Direct and Indirect Effects of Protist Predation on Population Size Structure of a Bacterial Strain with High Phenotypic Plasticity journal January 2006
Changes of traits in a bacterial population associated with protozoal predation journal December 1990
Utilization of acidic amino acids and their amides by pseudomonads: role of periplasmic glutaminase-asparaginase journal February 2003
Reaching out in anticipation: bacterial membrane extensions represent a permanent investment in polysaccharide sensing and utilization journal May 2021
A Kinase-Phosphatase Switch Transduces Environmental Information into a Bacterial Cell Cycle Circuit journal December 2016
Morphological plasticity as a bacterial survival strategy journal February 2008
Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil journal June 2020
Phosphate solubilizing bacteria and their role in plant growth promotion journal October 1999
Expression of Phi11 Gp07 Causes Filamentation in Escherichia coli journal April 2018
Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus journal August 1998
Novel Assay Reveals Multiple Pathways Regulating Stress-Induced Accumulations of Inorganic Polyphosphate in Escherichia coli journal April 1998
Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. journal August 1994
Survival and Filamentation of Salmonella enterica Serovar Enteritidis PT4 and Salmonella enterica Serovar Typhimurium DT104 at Low Water Activity journal April 2000
Enhanced Production of Recombinant Proteins in Escherichia coli by Filamentation Suppression journal February 2003
Elongation Correlates with Nutrient Deprivation in Pseudomonas aeruginosa Unsaturated Biofilms journal June 2002
Grazing Pressure by a Bacterivorous Flagellate Reverses the Relative Abundance of Comamonas acidovorans PX54 and Vibrio Strain CB5 in Chemostat Cocultures journal May 1998
Rapid β-lactam-induced lysis requires successful assembly of the cell division machinery journal December 2009
Emergence of antibiotic resistance from multinucleated bacterial filaments journal December 2014
Paraburkholderia panacihumi sp. nov., an isolate from ginseng-cultivated soil, is antagonistic against root rot fungal pathogen journal June 2018
Evaluation of the Role of the opgGH Operon in Yersinia pseudotuberculosis and Its Deletion during the Emergence of Yersinia pestis journal September 2015
Complete Genome Sequence of the Plant Growth-Promoting Endophyte Burkholderia phytofirmans Strain PsJN journal May 2011
Filamentous bulking sludge—a critical review journal February 2004
A Comprehensive, CRISPR-based Functional Analysis of Essential Genes in Bacteria journal June 2016
Cellular Changes Accompanying the Swarming of Proteus Mirabilis: ii. Observations of Stained Organisms journal February 1966
A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci: Filamentation of Lactococcus lactis journal December 2010
Phenolic acid-degrading Paraburkholderia prime decomposition in forest soil journal March 2021
The ecology of heterogeneity: soil bacterial communities and C dynamics journal March 2020
Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence: Surface-responsive gene expression journal November 2010
The Selective Value of Bacterial Shape journal September 2006
Filamentation initiated by Cas2 and its association with the acquisition process in cells journal September 2019
Impact of Matric Potential and Pore Size Distribution on Growth Dynamics of Filamentous and Non-Filamentous Soil Bacteria journal December 2013
Cryptic-Prophage-Encoded Small Protein DicB Protects Escherichia coli from Phage Infection by Inhibiting Inner Membrane Receptor Proteins journal December 2019
Effect of Bacterial Cell Shape on Transport of Bacteria in Porous Media journal July 1995
Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies journal January 2014
Use of a gnotobiotic plant assay for assessing root colonization and mineral phosphate solubilization by Paraburkholderia bryophila Ha185 in association with perennial ryegrass (Lolium perenne L.) journal March 2018
Phosphate-solubilizing Pseudomonas putida can influence the rhizobia–legume symbiosis journal December 2006
Comparative Analysis of Myxococcus Predation on Soil Bacteria journal October 2010
Successful Predation of Filamentous Bacteria by a Nanoflagellate Challenges Current Models of Flagellate Bacterivory journal January 2004
Ultraviolet Radiation Induces Filamentation in Bacterial Assemblages from North Andean Patagonian Lakes journal June 2010
The Ctp Type IVb Pilus Locus of Agrobacterium tumefaciens Directs Formation of the Common Pili and Contributes to Reversible Surface Attachment journal August 2014
More than a Tad: spatiotemporal control of Caulobacter pili journal April 2018
Oscillatory growth of fungal hyphae in wood cell walls journal March 1985
Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa journal April 2008
The Kil Peptide of Bacteriophage λ Blocks Escherichia coli Cytokinesis via ZipA-Dependent Inhibition of FtsZ Assembly journal March 2014
Bacterial filamentation accelerates colonization of adhesive spots embedded in biopassive surfaces journal December 2013
Bacterial cell division as a target for new antibiotics journal October 2013
Short-term variations in specific biovolumes of different bacterial forms in aquatic ecosystems journal December 1991
KBase: The United States Department of Energy Systems Biology Knowledgebase journal July 2018
Morphological and ultrastructural changes in bacterial cells as an indicator of antibacterial mechanism of action journal July 2016
Degradation of native wheat straw lignin by Streptomyces viridosporus T7A journal July 2012
The microbial habitat in soil: Scale, heterogeneity and functional consequences journal May 2017
Modified Virulence of Antibiotic-Induced Burkholderia pseudomallei Filaments journal March 2005
Aqueous extract of Hibiscus sabdariffa inhibits pedestal induction by enteropathogenic E. coli and promotes bacterial filamentation in vitro journal March 2019
The contentious nature of soil organic matter journal November 2015
Model for regulation of Escherichia coli DNA repair functions. journal June 1975
DNA and Polyphosphate in Directed Proteolysis for DNA Replication Control journal October 2020
Spatiotemporal distribution of different extracellular polymeric substances and filamentation mediate Xylella fastidiosa adhesion and biofilm formation journal April 2015
Filamentation and restoration of normal growth in Escherichia coli using a combined CRISPRi sgRNA/antisense RNA approach journal September 2018
Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba journal April 2007
Differential proteomics and physiology of Pseudomonas putida KT2440 under filament-inducing conditions journal November 2012
A Metabolic Sensor Governing Cell Size in Bacteria journal July 2007
Cytoplasmic steps of peptidoglycan biosynthesis journal March 2008
Chirality in microbial biofilms is mediated by close interactions between the cell surface and the substratum journal April 2017
Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms journal June 2019
Interactions and Self-Organization in the Soil-Microbe Complex journal June 2004
Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties journal May 2005
Considering the Lives of Microbes in Microbial Communities journal April 2018
Size Laws and Division Ring Dynamics in Filamentous Escherichia coli cells journal March 2018
Factors Influencing Filament Length of Methanospirillum hungatii journal June 1979
Filamentation promotes F'lac loss in Escherichia coli K12 journal October 1992
“Living” dynamics of filamentous bacteria on an adherent surface under hydrodynamic exposure journal June 2017
Behaviours of log phase cultures of eight strains of Escherichia coli incubated at temperatures of 2, 6, 8 and 10 °C journal November 2007
Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana journal February 2009
Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization journal February 2011
Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing journal September 2018
Bacterial preferences of the bacterivorous soil nematode Cephalobus brevicauda (Cephalobidae): Effect of bacterial type and size journal April 2007
MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis journal June 2016
Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana journal September 2020
Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis: Cell division suppressor in the B. subtilis SOS system journal February 2003
Seasonal dynamics of crustacean zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake journal February 1995
A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism journal July 2013
Enrichment of persisters enabled by a ß-lactam-induced filamentation method reveals their stochastic single-cell awakening journal November 2019