Abstract
Members of the Flavobacterium genus are widely distributed in nature where they are often associated with the capacity to degrade complex organic compounds. A myriad of recent studies indicate that the class Flavobacteria, and specifically the genus Flavobacterium, represent a significant fraction of root- and leaf-associated microbiomes in a broad range of plant species. Several of these studies have shown that the relative abundance of members of this genus increases substantially along the soil, rhizosphere, and rhizoplane continuum, indicating a specialized capacity to proliferate in plant environments and suggesting a role in plant functioning. Unlike other plant-associated genera such as Pseudomonas and Bacillus that have been exhaustively documented, little is known about the ecology of Flavobacteriumstrains in plant environments. This chapter summarizes current knowledge of Flavobacteriumstrains in plant habitats. It explores their abundance and diversity in the rhizosphere and the phyllosphere of a large range of plant species, elucidates the potential role of unique flavobacterial gliding-motility and gliding-secretion mechanisms in plant-Flavobacterium interactions, and explores the potential role of Flavobacteriumstrains in plant growth and protection.
Keywords
- Glycoside Hydrolase
- Endophytic Bacterial Community
- Flavobacterium Genus
- Rhizosphere Competence
- Rhizosphere Microbiome
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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References
Ahmad JS, Baker R (1987) Rhizosphere competence of Trichoderma harzianum. Phytopathology 77:182–189
Aleklett K, Leff J, Fierer N, Hart M (2015) Wild plant species growing closely connected in a subalpine meadow host distinct root-associated bacterial communities. Peerj 3:19
Alexander BJR, Stewart A (2001) Glasshouse screening for biological control agents of Phytophthora cactorum on apple (Malus domestica). N Z J Crop Hortic Sci 29:159–169
Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528(7582):364–369
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338
Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685
Bernardet JF, Bowman JP (2006) The genus Flavobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, New York
Bernardet JF, Bowman JP (2011) Genus I. Flavobacterium Bergey et al. 1923. In: Whitman W, (ed) Bergey’s manual of systematic bacteriology, 2 edn. The Williams & Wilkins Co, Baltimore
Bernardet JF, Nakagawa Y (2006) An introduction to the family Flavobacteriaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, New York
Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329
Bringhurst RM, Cardon ZG, Gage DJ (2001) Galactosides in the rhizosphere: utilization by Sinorhizobium meliloti and development of a biosensor. Proc Natl Acad Sci 98:4540–4545
Bulgarelli D, Rott M, Schlaeppi K, Van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800
Cardinale M, Grube M, Erlacher A, Quehenberger J, BERG G (2015) Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environ Microbiol 17:239–252
Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant-Microbe Interact 28:1049–1058
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803
Christensen P (1977) Synonymy of Flavobacterium pectinovorum Dorey with Cytophaga johnsonae Stanier. Int J Syst Bacteriol 27:122–132
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2015) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209(2):798–811
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697
De Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant-Microbe Interact 15:1173–1180
Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249
Flynn B, Graham A, Scott N, Layzell DB, Dong ZM (2014) Nitrogen fixation, hydrogen production and N2O emissions. Can J Plant Sci 94:1037–1041
Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390
Garbeva P, Van Elsas J, Van Veen J (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32
Georges AA, El-Swais H, Craig SE, Li WK, Walsh DA (2014) Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J 8:1301
Graber ER, Harel YM, Kolton M, Cytryn E, Silber A, David DR, Tsechansky L, Borenshtein M, Elad Y (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil 337:481–496
Gunasinghe WKRN, Karunaratne AM (2009) Interactions of Colletotrichum musae and Lasiodiplodia theobromae and their biocontrol by Pantoea agglomerans and Flavobacterium sp in expression of crown rot of “Embul” banana. Biocontrol 54:587–596
Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G, Lebeis S, Mchardy AC, Dangl JL, Knight R, Ley R (2015) Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–616
Haldar S, Choudhury SR, Sengupta S (2011) Genetic and functional diversities of bacterial communities in the rhizosphere of Arachis hypogaea. Antonie Van Leeuwenhoek 100:161–170
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320
Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14
Hebbar P, Berge O, Heulin T, Singh SP (1991) Bacterial antagonists of sunflower (Helianthus-Annuus L) fungal pathogens. Plant Soil 133:131–140
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl Environ Microbiol 76:8117–8125
Jarrell KF, Mcbride MJ (2008) The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol 6:466–476
Johansen JE, Binnerup SJ (2002) Contribution of Cytophaga-like bacteria to the potential of turnover of carbon, nitrogen, and phosphorus by bacteria in the rhizosphere of barley (Hordeum vulgare L.). Microb Ecol 43:298–306
Johansen JE, Nielsen P, Binnerup SJ (2009) Identification and potential enzyme capacity of Flavobacteria isolated from the rhizosphere of barley (Hordeum vulgare L.). Can J Microbiol 55:234–241
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33
Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8:634–644
Kharade SS, Mcbride MJ (2015) Flavobacterium johnsoniae PorV is required for secretion of a subset of proteins targeted to the type IX secretion system. J Bacteriol 197:147–158
Kinkel LL, Bakker MG, Schlatter DC (2011) A coevolutionary framework for managing disease-suppressive soils. Annu Rev Phytopathol 49:47–67
Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, Von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390
Kolton M, Harel YM, Pasternak Z, Graber ER, Elad Y, Cytryn E (2011) Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl Environ Microbiol 77:4924–4930
Kolton M, Green SJ, Harel YM, Sela N, Elad Y, Cytryn E (2012) Draft genome sequence of Flavobacterium sp strain F52, isolated from the rhizosphere of bell pepper (Capsicum annuum L. cv. Maccabi). J Bacteriol 194:5462–5463
Kolton M, Sela N, Elad Y, Cytryn E (2013) Comparative genomic analysis indicates that niche adaptation of terrestrial flavobacteria is strongly linked to plant glycan metabolism. PLoS One 8:11
Kolton M, Frenkel O, Elad Y, Cytryn E (2014) Potential role of flavobacterial gliding-motility and type IX secretion system complex in root colonization and plant defense. Mol Plant-Microbe Interact 27:1005–1013
Kuczynski J, Lauber CL, Walters WA, Parfrey LW, Clemente JC, Gevers D, Knight R (2012) Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 13:47–58
Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, Mcdonald M, Malfatti S, Del Rio TG, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864
Leff JW, Fierer N (2013) Bacterial communities associated with the surfaces of fresh fruits and vegetables. PLoS One 8:e59310
Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401
Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883
Lugtenberg BJJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13
Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, LEY RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Maimaiti J, Zhang Y, Yang J, Cen YP, Layzell DB, Peoples M, Dong Z (2007) Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environ Microbiol 9:435–444
Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166
Mark GL, Dow JM, Kiely PD, Higgins H, Haynes J, Baysse C, Abbas A, Foley T, Franks A, Morrissey J (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci U S A 102:17454–17459
Mcbride MJ (2004) Cytophaga-Flavobacterium gliding motility. J Mol Microbiol Biotechnol 7:63–71
Mcbride MJ, Nakane D (2015) Flavobacterium gliding motility and the type IX secretion system. Curr Opin Microbiol 28:72–77
Mcbride MJ, Zhu YT (2013) Gliding motility and Por Secretion System genes are widespread among members of the phylum Bacteroidetes. J Bacteriol 195:270–278
Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van Der Voort M, Schneider JH, Piceno YM, Desantis TZ, Andersen GL, Bakker PA (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Morris C, Kinkel L, Lindow S, Hecht-Poinar E, Elliott V (2002) Fifty years of phyllosphere microbiology: significant contributions to research in related fields. Phyllosph Microbiol 365–375
Nakane D, Sato K, Wada H, Mcbride MJ, Nakayama K (2013) Helical flow of surface protein required for bacterial gliding motility. Proc Natl Acad Sci U S A 110:11145–11150
Nan B, Mcbride MJ, Chen J, Zusman DR, Oster G (2014) Bacteria that glide with helical tracks. Curr Biol 24:R169–R173
Ofek M, Voronov-Goldman M, Hadar Y, Minz D (2014) Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs. active communities. Environ Microbiol 16:2157–2167
Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y, Minz D (2014) Niche and host-associated functional signatures of the root surface microbiome. Nat Commun 5:9
Olsson S, Persson P (1999) The composition of bacterial populations in soil fractions differing in their degree of adherence to barley roots. Appl Soil Ecol 12:205–215
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, LEY RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci 110:6548–6553
Peterson SB, Dunn AK, Klimowicz AK, Handelsman J (2006) Peptidoglycan from Bacillus cereus mediates commensalism with rhizosphere bacteria from the Cytophaga-Flavobacterium group. Appl Environ Microbiol 72:5421–5427
Qin Y, Fu Y, Dong C, Jia N, Liu H (2016) Shifts of microbial communities of wheat (Triticum aestivum L.) cultivation in a closed artificial ecosystem. Appl Microbiol Biotechnol 100:1–11
Reichenbach H, Kohl W, Böttger-Vetter A, Achenbach H (1980) Flexirubin-type pigments in Flavobacterium. Arch Microbiol 126:291–293
Reinhold-Hurek B, Buenger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. In: Vanalfen NK (ed) Annual review of phytopathology, vol 53
Rodriguez-Navarro DN, Dardanelli MS, Ruiz-Sainz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136
Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2:500–506
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351
Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57
Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556
Ruinen J (1956) Occurrence of Beijerinckia species in the ‘phyllosphere’ Nature 177: 220–221
Sato K, Naito M, Yukitake H, Hirakawa H, Shoji M, McBride MJ, Rhodes RG, Nakayama K (2010) A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci 107:276–281
Sang MK, Kim KD (2012) The volatile-producing Flavobacterium johnsoniae strain GSE09 shows biocontrol activity against Phytophthora capsici in pepper. J Appl Microbiol 113:383–398
Sang MK, Chun SC, Kim KD (2008) Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol Control 46:424–433
Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, Van Overbeek L, Brar D, Van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36
Shi SJ, Nuccio E, Herman DJ, Rijkers R, Estera K, Li JB, Da Rocha UN, He ZL, Pett-Ridge J, Brodie EL, Zhou JZ, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. Mbio 6:8
Shrivastava A, Berg HC (2015) Towards a model for Flavobacterium gliding. Curr Opin Microbiol 28:93–97
Shrivastava A, Johnston JJ, Van Baaren JM, Mcbride MJ (2013) Flavobacterium johnsoniae GldK, GldL, GldM, and SprA are required for secretion of the cell surface gliding motility adhesins SprB and RemA. J Bacteriol 195:3201–3212
Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751
Soltani A-A, Khavazi K, Asadi-Rahmani H, Omidvari M, Abaszadeh Dahaji P, Mirhoseyni H (2010) Plant growth promoting characteristics in some Flavobacterium spp. Isolated from soils of Iran. J Agric Sci 2:4
Stanier RY (1947) Studies on non-fruiting myxobacteria. I. Cytophaga johnsonae, n. sp., a chitin-decomposing myxobacterium. J Bacteriol 53:297–315
Sudheesh PS, Al-Ghabshi A, Al-Mazrooei N, Al-Habsi S (2012) Comparative pathogenomics of bacteria causing infectious diseases in fish. Int J Evol Biol 2012:16
Tian Y, Gao L (2014) Bacterial diversity in the rhizosphere of cucumbers grown in soils covering a wide range of cucumber cropping histories and environmental conditions. Microb Ecol 68:794–806
Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AI (2007a) Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res 162:69–76
Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2007b) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664
Umamaheswari T, Anbukkarasi K, Hemalatha T, Chendrayan K (2013) Studies on phytohormone producing ability of indigenous endophytic bacteria isolated from tropical legume crops. Int J Curr Microbiol Appl Sci 2:127–136
Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840
Whipps JM, Lynch JM (1986) The influence of the rhizosphere on crop productivity. In: Marshall KC (ed) Advances in microbial ecology. Springer, Boston
Wiewióra B, Żurek G, Pańka D (2015) Is the vertical transmission of Neotyphodium lolii in perennial ryegrass the only possible way to the spread of endophytes? PLoS One 10:e0117231
Yoon J-H, Kang S-J, Oh T-K (2006) Flavobacterium soli sp. nov., isolated from soil. Int J Syst Evol Microbiol 56:997–1000
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6:e02527–14
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735
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Kolton, M., Erlacher, A., Berg, G., Cytryn, E. (2016). The Flavobacterium Genus in the Plant Holobiont: Ecological, Physiological, and Applicative Insights. In: Castro-Sowinski, S. (eds) Microbial Models: From Environmental to Industrial Sustainability. Microorganisms for Sustainability, vol 1. Springer, Singapore. https://doi.org/10.1007/978-981-10-2555-6_9
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