Skip to main content
Log in

The genus Caulobacter and its role in plant microbiomes

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Recent omics approaches have revealed the prevalent microbial taxa that constitute the microbiome of various plant species. Across global scales and environmental conditions, strains belonging to the bacterial genus Caulobacter have consistently been found in association with various plant species. Aligned with agroecological relevance and biotechnological advances, many scientific communications have demonstrated that several Caulobacter strains (spanning several Caulobacter species) harbor the potential to enhance plant biomass for various plant species ranging from Arabidopsis to Citrullus and Zea mays. In the past several years, co-occurrence data have driven mechanistically resolved communications about select Caulobacter–plant interactions. Given the long-standing history of Caulobacter as a model organism for cell cycle regulation, genetic studies, and the prevalence of Caulobacter species in various plant microbiomes, the genus Caulobacter offers researchers a unique opportunity to leverage for investigating plant–microbe interactions and realizing targeted biotechnological applications. In this review, recent developments regarding Caulobacter–plant interactions are presented in terms of model utility for future biotechnological investigations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

All relevant data are within the manuscript.

Code availability

Not applicable.

References

  • Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, Weigel D, Kemen EM (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14(1):e1002352

    PubMed  PubMed Central  Google Scholar 

  • Ankati S, Podile AR (2019) Metabolites in the root exudates of groundnut change during interaction with plant growth promoting rhizobacteria in a strain-specific manner. J Plant Physiol 243:153057

    CAS  PubMed  Google Scholar 

  • Ash K, Brown T, Watford T, Scott LE, Stephens C, Ely B (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biology 4(10):140128

    PubMed  PubMed Central  Google Scholar 

  • Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, El Enshasy H (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13(3):1140

    CAS  Google Scholar 

  • Bentkowski P, Van Oosterhout C, Mock T (2015) A model of genome size evolution for prokaryotes in stable and fluctuating environments. Genome Biol Evol 7(8):2344–2351

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berrios L (2021) Complete genome sequence of the plant-growth-promoting bacterium Caulobacter segnis CBR1. Curr Microbiol 28:1–8

    Google Scholar 

  • Berrios L (2022) Plant-growth-promoting Caulobacter strains isolated from distinct plant hosts share conserved genetic factors involved in beneficial plant–bacteria interactions. Arch Microbiol 204(1):1

    Google Scholar 

  • Berrios L, Ely B (2019) The isolation and characterization of Kronos, a novel Caulobacter rhizosphere phage that is similar to lambdoid phages. Curr Microbiol 76(5):558–565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berrios L, Ely B (2020) Plant growth enhancement is not a conserved feature in the Caulobacter genus. Plant Soil 449(1):81–95

    CAS  Google Scholar 

  • Berrios L, Ely B (2021) Genes related to redox and cell curvature facilitate interactions between Caulobacter strains and Arabidopsis. PloS One 16(4):e0249227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 20:219

    Google Scholar 

  • Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL, Land ML, Lu TY, Schadt CW, Doktycz MJ, Pelletier DA (2012) Twenty-one genome sequences from Pseudomonas species and 19 genome sequences from diverse bacteria isolated from the rhizosphere and endosphere of Populus deltoides. J Bacteriol 194:5991–5993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brzoska RM, Bollmann A (2016) The long-term effect of uranium and pH on the community composition of an artificial consortium. FEMS Microbiol Ecol 92(1):fiv158

    PubMed  Google Scholar 

  • Chen MY, Teng WK, Zhao L, Hu CX, Zhou YK, Han BP, Song LR, Shu WS (2021) Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation. ISME J 15(1):211–227

    PubMed  Google Scholar 

  • Cheng Z, Lei S, Li Y, Huang W, Ma R, Xiong J, Zhang T, Jin L, Xu X, Tian B (2020) Revealing the variation and stability of bacterial communities in tomato rhizosphere microbiota. Microorganisms 8(2):170

    Article  CAS  PubMed Central  Google Scholar 

  • Cobo-Simón M, Tamames J (2017) Relating genomic characteristics to environmental preferences and ubiquity in different microbial taxa. BMC Genom 18(1):1–1

    Google Scholar 

  • Deng S, Wipf HM, Pierroz G, Raab TK, Khanna R, Coleman-Derr D (2019) A plant growth-promoting microbial soil amendment dynamically alters the strawberry root bacterial microbiome. Sci Rep 9(1):1–5

    Google Scholar 

  • Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky OA, Mieszkin S (2018) Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev 42(3):335–352

    CAS  PubMed  Google Scholar 

  • Ely B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204:372–384

    CAS  PubMed  Google Scholar 

  • Ely B, Wilson K, Ross K, Ingram D, Lewter T, Herring J, Duncan D, Aikins A, Scott D (2019) Genome comparisons of wild isolates of Caulobacter crescentus reveal rates of inversion and horizontal gene transfer. Curr Microbiol 76(2):159–167

    CAS  PubMed  Google Scholar 

  • Erlandson S, Wei X, Savage J, Cavender-Bares J, Peay K (2018) Soil abiotic variables are more important than Salicaceae phylogeny or habitat specialization in determining soil microbial community structure. Mol Ecol 27(8):2007–2024

    PubMed  Google Scholar 

  • Fadiji AE, Kanu JO, Babalola OO (2021) Metagenomic profiling of rhizosphere microbial community structure and diversity associated with maize plant as affected by cropping systems. Int Microbiol 5:1–1

    Google Scholar 

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10(8):538–550

    CAS  PubMed  Google Scholar 

  • Finkel OM, Salas-González I, Castrillo G, Conway JM, Law TF, Teixeira PJ, Wilson ED, Fitzpatrick CR, Jones CD, Dangl JL (2020) A single bacterial genus maintains root growth in a complex microbiome. Nat 587(7832):103–108

    CAS  Google Scholar 

  • Gao M, Xiong C, Gao C, Tsui CK, Wang MM, Zhou X, Zhang AM, Cai L (2021) Disease-induced changes in plant microbiome assembly and functional adaptation. Microbiome 9(1):1–8

    CAS  Google Scholar 

  • García-Bayona L, Guo MS, Laub MT (2017) Contact-dependent killing by Caulobacter crescentus via cell surface-associated, glycine zipper proteins. Elife 6:e24869

    PubMed  PubMed Central  Google Scholar 

  • Giovannoni SJ, Thrash JC, Temperton B (2014) Implications of streamlining theory for microbial ecology. ISME J 8(8):1553–1565

    PubMed  PubMed Central  Google Scholar 

  • Gqozo MP, Bill M, Siyoum N, Labuschagne N, Korsten L (2020) Fungal diversity and community composition of wheat rhizosphere and non-rhizosphere soils from three different agricultural production regions of South Africa. Appl Soil Ecol 151:103543

    Google Scholar 

  • Gutiérrez-García K, Bustos-Díaz ED, Corona-Gómez JA, Ramos-Aboites HE, Sélem-Mojica N, Cruz-Morales P, Pérez-Farrera MA, Barona-Gómez F, Cibrián-Jaramillo A (2019) Cycad coralloid roots contain bacterial communities including cyanobacteria and Caulobacter spp. that encode niche-specific biosynthetic gene clusters. Genome Biol Evol 11(1):319–334

    PubMed  Google Scholar 

  • Hannula SE, Kielak AM, Steinauer K, Huberty M, Jongen R, De Long JR, Heinen R, Bezemer TM (2019) Time after time: temporal variation in the effects of grass and forb species on soil bacterial and fungal communities. MBio 10(6):e02635-e2719

    PubMed  PubMed Central  Google Scholar 

  • Hershey DM, Fiebig A, Crosson S (2021) Flagellar perturbations activate adhesion through two distinct pathways in Caulobacter crescentus. MBio 12(1):e03266-e3320

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hottes AK, Shapiro L, McAdams HH (2005) DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 58(5):1340–1353

    CAS  PubMed  Google Scholar 

  • Hung D, McAdams H, Shapiro L (1999) Regulation of the Caulobacter cell cycle. Prokaryotic Dev 14:361–378

    Google Scholar 

  • Kominoski JS, Marczak LB, Richardson JS (2011) Riparian forest composition affects stream litter decomposition despite similar microbial and invertebrate communities. Ecology 92(1):151–159

    PubMed  Google Scholar 

  • Laub MT, Chen SL, Shapiro L, McAdams HH (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci USA 99(7):4632–4637

    CAS  PubMed  PubMed Central  Google Scholar 

  • Letten AD, Stouffer DB (2019) The mechanistic basis for higher-order interactions and non-additivity in competitive communities. Ecol Lett 22(3):423–436

    PubMed  Google Scholar 

  • Levy A, Gonzalez IS, Mittelviefhaus M, Clingenpeel S, Paredes SH, Miao J, Wang K, Devescovi G, Stillman K, Monteiro F, Alvarez BR (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50(1):138–150

    CAS  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo D, Langendries S, Mendez SG, De Ryck J, Liu D, Beirinckx S, Willems A, Russinova E, Debode J, Goormachtig S (2019) Plant growth promotion driven by a novel Caulobacter strain. Mol Plant-Microbe Interact 32(9):1162–1174

    CAS  PubMed  Google Scholar 

  • Martínez-Arias C, Sobrino-Plata J, Macaya-Sanz D, Aguirre NM, Collada C, Gil L, Martín JA, Rodríguez-Calcerrada J (2020) Changes in plant function and root mycobiome caused by flood and drought in a riparian tree. Tree Physiol 40(7):886–903

    PubMed  Google Scholar 

  • Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145(15):dev164376

    PubMed  Google Scholar 

  • Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2014) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50(2):249–62

    CAS  Google Scholar 

  • Nemec P, Bystrický V (1962) Peculiar morphology of some microorganisms accompanying diatomaceae preliminary report. J General Appl Microbiol 8(3):121–129

    Google Scholar 

  • Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen J, Heidelberg JF, Alley MR, Ohta N, Maddock JR, Potocka I (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98(7):4136–4141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noirot-Gros MF, Shinde S, Larsen PE, Zerbs S, Korajczyk PJ, Kemner KM, Noirot PH (2018) Dynamics of aspen roots colonization by Pseudomonads reveals strain-specific and mycorrhizal-specific patterns of biofilm formation. Front Microbiol 9:853

    PubMed  PubMed Central  Google Scholar 

  • Owen D, Williams AP, Griffith GW, Withers PJ (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl Soil Ecol 86:41–54

    Google Scholar 

  • Patel S, Fletcher B, Scott DC, Ely B (2015) Genome sequence and phenotypic characterization of Caulobacter segnis. Curr Microbiol 70(3):355–363

    CAS  PubMed  Google Scholar 

  • Pereira SI, Monteiro C, Vega AL, Castro PM (2016) Endophytic culturable bacteria colonizing Lavandula dentata L. plants: isolation, characterization and evaluation of their plant growth-promoting activities. Ecol Eng 87:91–97

    Google Scholar 

  • Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28(3):231–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao Q, Wang F, Zhang J, Chen Y, Zhang C, Liu G, Zhang H, Ma C, Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Sci Rep 7(1):1

    Google Scholar 

  • Rodríguez-Gijón A, Nuy JK, Mehrshad M, Buck M, Schulz F, Woyke T, Garcia SL (2021) A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy. Front Microbiol 18:4194

    Google Scholar 

  • Sanchez-Gorostiaga A, Bajić D, Osborne ML, Poyatos JF, Sanchez A (2019) High-order interactions distort the functional landscape of microbial consortia. PLoS Biol 17(12):e3000550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sangermani M, Hug I, Sauter N, Pfohl T, Jenal U (2019) Tad pili play a dynamic role in Caulobacter crescentus surface colonization. MBio 10(3):e01237-e1319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena P, Misra N (2010) Remediation of heavy metal contaminated tropical land. Soil heavy metals. Springer, Berlin, pp 431–477

    Google Scholar 

  • Scott D, Ely B (2016) Conservation of the essential genome among Caulobacter and Brevundimonas species. Curr Microbiol 72(5):503–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh M, Bhasin S, Madan N, Suyal DC, Soni R, Singh D (2021) Bioinoculants for agricultural sustainability. Microbiological activity for soil and plant health management. Springer, Singapore, pp 629–641

    Google Scholar 

  • Skerker JM, Laub MT (2004) Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2(4):325–337

    CAS  PubMed  Google Scholar 

  • Sommer JM, Newton AU (1989) Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus. J Bacteriol 171(1):392–401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taffner J, Bergna A, Cernava T, Berg G (2020) Tomato-associated archaea show a cultivar-specific rhizosphere effect but an unspecific transmission by seeds. Phytobiomes J 4(2):133–141

    Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nat 418(6898):671–677

    CAS  Google Scholar 

  • Utturkar SM, Bollmann A, Brzoska RM, Klingeman DM, Epstein SE, Palumbo AV, Brown SD (2013) Draft genome sequence for Caulobacter sp. strain OR37, a bacterium tolerant to heavy metals. Genome Announc. https://doi.org/10.1128/genomeA.00322-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Qin Y, Kot W, Zhang F, Zheng S, Wang G, Hansen LH, Rensing C (2016) Genome sequence of selenium-solubilizing bacterium Caulobacter vibrioides T5M6. Genome Announc 4(1):e01721-e1815

    PubMed  PubMed Central  Google Scholar 

  • Wang Q, Liu J, Li H, Yang S, Körmöczi P, Kereszt A, Zhu H (2018) Nodule-specific cysteine-rich peptides negatively regulate nitrogen-fixing symbiosis in a strain-specific manner in Medicago truncatula. Mol Plant-Microbe Interact 31(2):240–248

    CAS  PubMed  Google Scholar 

  • Wilhelm RC (2018) Following the terrestrial tracks of Caulobacter-redefining the ecology of a reputed aquatic oligotroph. ISME J 12(12):3025–3037

    PubMed  PubMed Central  Google Scholar 

  • Yang E, Sun L, Ding X, Sun D, Liu J, Wang W (2019) Complete genome sequence of Caulobacter flavus RHGG3 T, a type species of the genus Caulobacter with plant growth-promoting traits and heavy metal resistance. 3 Biotech 9(2):42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Wei S, Su D, Zhang Z, Chen S, Luo Z, Shen X, Lai Y, Jamil A, Tong J, Cui X (2020) Comparison of the rhizosphere soil microbial community structure and diversity between powdery mildew-infected and noninfected strawberry plants in a greenhouse by high-throughput sequencing technology. Curr Microbiol 77(8):1724–1736

    CAS  PubMed  Google Scholar 

  • Zhang K, Adams JM, Shi Y, Yang T, Sun R, He D, Ni Y, Chu H (2017) Environment and geographic distance differ in relative importance for determining fungal community of rhizosphere and bulk soil. Environ Microbiol 19(9):3649–3659

    PubMed  Google Scholar 

  • Zuo J, Zu M, Liu L, Song X, Yuan Y (2021) Composition and diversity of bacterial communities in the rhizosphere of the Chinese medicinal herb Dendrobium. BMC Plant Biol. https://doi.org/10.1186/s12870-021-02893-y

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was funded in part by a National Science Foundation PRFB Grant (2109481) awarded to LB. The funders did not contribute to the design of the experiments, data collection, analyses, decision to publish, or the preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

LB: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing (original draft), writing (review and editing).

Corresponding author

Correspondence to Louis Berrios.

Ethics declarations

Conflict of interest

The authors have declared that no competing interests exist.

Ethical approval

All analyses were based on previous published studies; thus, no ethical approval and patient consent are required.

Research involving human and animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berrios, L. The genus Caulobacter and its role in plant microbiomes. World J Microbiol Biotechnol 38, 43 (2022). https://doi.org/10.1007/s11274-022-03237-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-022-03237-0

Keywords

Navigation