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Diversity and ecology of oxalotrophic bacteria

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Abstract

Oxalate is present in environments as diverse as soils or gastrointestinal tracts. This organic acid can be found as free acid or forming metal salts (e.g. calcium, magnesium). Oxalotrophy, the ability to use oxalate as carbon and energy sources, is mainly the result of bacterial catabolism, which can be either aerobic or anaerobic. Although some oxalotrophic bacterial strains are commonly used as probiotics, little is known about the diversity and ecology of this functional group. This review aims at exploring the taxonomic distribution and the phylogenetic diversity of oxalotrophic bacteria across biomes. In silico analyses were conducted using the two key enzymes involved in oxalotrophy: formyl-coenzyme A (CoA) transferase (EC 2.8.3.16) and oxalyl-CoA decarboxylase (EC 4.1.1.8), encoded by the frc and oxc genes, respectively. Our analyses revealed that oxalate-degrading bacteria are restricted to three phyla, namely Actinobacteria, Firmicutes and Proteobacteria and originated from terrestrial, aquatic and clinical environments. Diversity analyses at the protein level suggest that total Oxc diversity is more constrained than Frc diversity and that bacterial oxalotrophic diversity is not yet fully described. Finally, the contribution of oxalotrophic bacteria to ecosystem functioning as well as to the carbon cycle is discussed.

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References

  • Abratt VR, Reid SJ (2010) Oxalate-degrading bacteria of the human gut as probiotics in the management of kidney stone disease. Adv Appl Microbiol 72:63–87

    Article  CAS  Google Scholar 

  • Anbazhagan K, Edward Raja C, Selvam GS (2007) Oxalotrophic Paracoccus alcaliphilus isolated from Amorphophallus sp. rhizoplane. World J Microbiol Biotechnol 23:1529–1535

    Article  CAS  Google Scholar 

  • Azcarate-Peril MA, Bruno-Bárcena JM, Hassan HM, Klaenhammer TR (2006) Transcriptional and functional analysis of oxalyl-coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes from Lactobacillus acidophilus. Appl Environ Microbiol 72:1891–1899

    Article  CAS  Google Scholar 

  • Bolan NS, Adriano DC, Curtin D (2003) Soil acidification and liming interactions with nutrient and heavy metal transformationand bioavailability. Adv Agron 78:215–272

    Article  CAS  Google Scholar 

  • Braissant O, Verrecchia EP, Aragno M (2002) Is the contribution of bacteria to terrestrial carbon budget greatly underestimated? Naturwissenschaften 89:366–370

    Article  CAS  Google Scholar 

  • Braissant O, Cailleau G, Aragno M, Verrecchia EP (2004) Biologically induced mineralization in the tree Milicia excelsa (Moraceae): its causes and consequences to the environment. Geobiology 2:59–66

    Article  CAS  Google Scholar 

  • Bravo D, Cailleau G, Bindschedler S, Simon A, Job D, Verrecchia E, Junier P (2013a) Isolation of oxalotrophic bacteria able to disperse on fungal mycelium. FEMS Microbiol Lett 348:157–166

    Article  CAS  Google Scholar 

  • Bravo D, Martin G, David MM, Cailleau G, Verrecchia E, Junier P (2013b) Identification of active oxalotrophic bacteria by Bromodeoxyuridine DNA labeling in a microcosm soil experiments. FEMS Microbiol Lett 348:103–111

    Article  CAS  Google Scholar 

  • Bravo D, Braissant O, Cailleau G, Verrecchia E, Junier P (2015) Isolation and characterization of oxalotrophic bacteria from tropical soils. Arch Microbiol 197:65–77

    Article  CAS  Google Scholar 

  • Cailleau G, Braissant O, Verrecchia EP (2004) Biomineralization in plants as a long-term carbon sink. Naturwissenschaften 91:191–194

    Article  CAS  Google Scholar 

  • Cailleau G, Braissant O, Verrecchia EP (2011) Turning sunlight into stone: the oxalate–carbonate pathway in a tropical tree ecosystem. Biogeosciences 8:1755–1767

    Article  CAS  Google Scholar 

  • Cailleau G, Mota M, Bindschedler S, Junier P, Verrecchia EP (2014) Detection of active oxalate–carbonate pathway ecosystems in the Amazon Basin: global implications of a natural potential C sink. Catena 116:132–141

    Article  CAS  Google Scholar 

  • Certini G, Corti G, Ugolini FC (2000) Vertical trends of oxalate concentration in two soils under Abies alba from Tuscany (Italy). J Plant Nutr Soil Sci 163:173–177

    Article  CAS  Google Scholar 

  • Créach V, Schricke MT, Bertru G, Mariotti A (1997) Stable isotopes and gut analyses to determine feeding relationships in saltmarsh macroconsumers. Estuar Coast Shelf Sci 44:599–611

    Article  Google Scholar 

  • Cromack K Jr, Sollins P, Todd RL, Fogel R, Todd AW, Fender WM, Crossley ME, Crossley DA Jr (1977) The role of oxalic acid and bicarbonate in calcium cycling by fungi and bacteria: some possible implications for soil animals. Ecol Bull 25:246–252

    CAS  Google Scholar 

  • Daniel SL, Pilsl C, Drake HL (2007) Anaerobic oxalate consumption by microorganisms in forest soils. Res Microbiol 158:303–309

    Article  CAS  Google Scholar 

  • De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  CAS  Google Scholar 

  • Dickman MB, Chet I (1998) Biodegradation of oxalic acid: a potential new approach to biological control. Soil Biol Biochem 30:1195–1197

    Article  CAS  Google Scholar 

  • Dutton MV, Evans CS (1996) Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can J Microbiol 42:881–895

    Article  CAS  Google Scholar 

  • Ee R, Yong D, Lim YL, Yin W-F, Chan K-G (2015) Complete genome sequence of oxalate-degrading bacterium Pandoraea vervacti DSM 23571(T). J Biotechnol 204:5–6

    Article  CAS  Google Scholar 

  • Folman LB, Klein Gunnewiek PJ, Boddy L, De Boer W (2008) Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil. FEMS Micriobiol Ecol 63:181–191

    Article  CAS  Google Scholar 

  • Franceschi VR, Nakata PA (2005) Calcium Oxalate in Plants: formation and Function. Annu Rev Plant Biol 56:41–71

    Article  CAS  Google Scholar 

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152

    Article  CAS  Google Scholar 

  • Gadd, G.M., 1999. Fungal Production of Citric and Oxalic Acid: Importance in Metal Speciation, Physiology and Biogeochemical Processes, in: Advances in Microbial Physiology. pp. 47–92

  • Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  CAS  Google Scholar 

  • Gadd GM, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X (2014) Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev 28:36–55

    Article  Google Scholar 

  • Garvie LAJ (2006) Decay of cacti and carbon cycling. Naturwissenschaften 93:114–118

    Article  CAS  Google Scholar 

  • Giardina S, Scilironi C, Michelotti A, Samuele A, Borella F, Daglia M, Marzatico F (2014) In vitro anti-inflammatory activity of selected oxalate-degrading probiotic bacteria: potential applications in the prevention and treatment of hyperoxaluria. J Food Sci 79:M384–M390

    Article  CAS  Google Scholar 

  • Guggiari M, Bloque R, Aragno M, Verrecchia E, Job D, Junier P (2011) Experimental calcium-oxalate crystal production and dissolution by selected wood-rot fungi. Int Biodeterior Biodegrad 65:803–809

    Article  CAS  Google Scholar 

  • Hervé V, Le Roux X, Uroz S, Gelhaye E, Frey-Klett P (2014) Diversity and structure of bacterial communities associated with Phanerochaete chrysosporium during wood decay. Environ Microbiol 16:2238–2252

    Article  CAS  Google Scholar 

  • Hess D, Coker DJ, Loutsch JM, Russ J (2008) Production of oxalates in vitro by microbes isolated from rock surfaces with prehistoric paints in the lower Pecos Region, Texas. Geoarchaeology 23:3–11

    Article  Google Scholar 

  • Hirai T, Subramaniam S (2004) Structure and transport mechanism of the bacterial oxalate transporter OxlT. Biophys J 87:3600–3607

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Kawamura K, Ikushima K (1993) Seasonal changes in the distribution of dicarboxylic acids in the urban atmosphere. Environ Sci Technol 27:2227–2235

    Article  CAS  Google Scholar 

  • Khammar N, Martin G, Ferro K, Job D, Aragno M, Verrecchia E (2009) Use of the frc gene as a molecular marker to characterize oxalate-oxidizing bacterial abundance and diversity structure in soil. J Microbiol Methods 76:120–127

    Article  CAS  Google Scholar 

  • Klenk H-P, Göker M (2010) En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol 33:175–182

    Article  CAS  Google Scholar 

  • Knutson DM, Hutchins AS, Cromack K (1980) The association of calcium oxalate-utilizing Streptomyces with conifer ectomycorrhizae. Antonie Van Leeuwenhoek 46:611–619

    Article  CAS  Google Scholar 

  • Koch M, Delmotte N, Ahrens CH, Omasits U, Schneider K, Danza F, Padhi B, Murset V, Braissant O, Vorholt JA, Hennecke H, Pessi G (2014) A link between arabinose utilization and oxalotrophy in Bradyrhizobium japonicum. Appl Environ Microbiol 80:2094–2101

    Article  CAS  Google Scholar 

  • Kost T, Stopnisek N, Agnoli K, Eberl L, Weisskopf L (2014) Oxalotrophy, a widespread trait of plant-associated Burkholderia species, is involved in successful root colonization of lupin and maize by Burkholderia phytofirmans. Front Microbiol 4:421

    Article  Google Scholar 

  • Lang E, Swiderski J, Stackebrandt E, Schumann P, Spröer C, Sahin N (2007) Herminiimonas saxobsidens sp. nov., isolated from a lichen-colonized rock. Int J Syst Evol Microbiol 57:2618–2622

    Article  CAS  Google Scholar 

  • Martin G, Guggiari M, Bravo D, Zopfi J, Cailleau G, Aragno M, Job D, Verrecchia E, Junier P (2012) Fungi, bacteria and soil pH: the oxalate-carbonate pathway as a model for metabolic interaction. Environ Microbiol 14:2960–2970

    Article  CAS  Google Scholar 

  • Marx CJ, Bringel F, Chistoserdova L, Moulin L, Farhan Ul Haque M, Fleischman DE, Gruffaz C, Jourand P, Knief C, Lee M-C, Muller EEL, Nadalig T, Peyraud R, Roselli S, Russ L, Goodwin LA, Ivanova N, Kyrpides N, Lajus A, Land ML, Médigue C, Mikhailova N, Nolan M, Woyke T, Stolyar S, Vorholt JA, Vuilleumier S (2012) Complete genome sequences of six strains of the genus Methylobacterium. J Bacteriol 194:4746–4748

    Article  CAS  Google Scholar 

  • Mela F, Fritsche K, de Boer W, van Veen JA, de Graaff LH, van den Berg M, Leveau JHJ (2011) Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J 5:1494–1504

    Article  CAS  Google Scholar 

  • Miller A, Dearing D (2013) The metabolic and ecological interactions of oxalate-degrading bacteria in the mammalian gut. Pathogens 2:636–652

    Article  CAS  Google Scholar 

  • Miller AW, Kohl KD, Dearing MD (2014) The gastrointestinal tract of the white-throated Woodrat (Neotoma albigula) harbors distinct consortia of oxalate-degrading bacteria. Appl Environ Microbiol 80:1595–1601

    Article  CAS  Google Scholar 

  • Mujinya BB, Mees F, Boeckx P, Bodé S, Baert G, Erens H, Delefortrie S, Verdoodt A, Ngongo M, Van Ranst E (2011) The origin of carbonates in termite mounds of the Lubumbashi area, D.R. Congo. Geoderma 165:95–105

    Article  CAS  Google Scholar 

  • Nakata PA (2011) The oxalic acid biosynthetic activity of Burkholderia mallei is encoded by a single locus. Microbiol Res 166:531–538

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2012). VEGAN: Community Ecology Package. R Package

  • Orellana LH, Rodriguez-R LM, Higgins S, Chee-Sanford JC, Sanford RA, Ritalahti KM, Löffler FE, Konstantinidis KT (2014) Detecting nitrous oxide reductase (NosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. MBio 5:e01193–14

    Article  CAS  Google Scholar 

  • R Development Core Team (2015) R: A Language and Environment for Statistical Computing

  • Rudnick MB, van Veen JA, de Boer W (2015) Oxalic acid: a signal molecule for fungus-feeding bacteria of the genus Collimonas? Environ Microbiol Rep 7:709–714

    Article  CAS  Google Scholar 

  • Sahin N (2003) Oxalotrophic bacteria. Res Microbiol 154:399–407

    Article  CAS  Google Scholar 

  • Sahin N, Gonzalez JM, Iizuka T, Hill JE (2010) Characterization of two aerobic ultramicrobacteria isolated from urban soil and a description of Oxalicibacterium solurbis sp. nov. FEMS Microbiol Lett 307:25–29

    Article  CAS  Google Scholar 

  • Schneider K, Skovran E, Vorholt JA (2012) Oxalyl-coenzyme A reduction to glyoxylate is the preferred route of oxalate assimilation in Methylobacterium extorquens AM1. J Bacteriol 194:3144–3155

    Article  CAS  Google Scholar 

  • Schoknecht JD, Keller HW (1977) Peridial composition of white fructifications in the Trichiales (Perichaena and Dianema). Can J Bot 55:1807–1819

    Article  CAS  Google Scholar 

  • Schoonbeek H, Jacquat-Bovet A-C, Mascher F, Métraux J-P (2007) Oxalate-degrading bacteria can protect Arabidopsis thaliana and crop plants against botrytis cinerea. Mol Plant-Microbe Interact 20:1535–1544

    Article  CAS  Google Scholar 

  • Smith RL, Oremland RS (1983) Anaerobic oxalate degradation: widespread natural occurrence in aquatic sediments. Appl Environ Microbiol 46:106–113

    CAS  Google Scholar 

  • Smith RL, Strohmaier FE, Oremland RS (1985) Isolation of anaerobic oxalate-degrading bacteria from freshwater lake sediments. Arch Microbiol 141:8–13

    Article  CAS  Google Scholar 

  • Stephens WE (2012) Whewellite and its key role in living systems. Geol Today 28:180–185

    Article  Google Scholar 

  • Stewart CS, Duncan SH, Cave DR (2004) Oxalobacter formigenes and its role in oxalate metabolism in the human gut. FEMS Microbiol, Lett

    Google Scholar 

  • Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution—a review. Geoderma 99:169–198

    Article  CAS  Google Scholar 

  • Svedruzić D, Jónsson S, Toyota CG, Reinhardt LA, Ricagno S, Lindqvist Y, Richards NGJ (2005) The enzymes of oxalate metabolism: unexpected structures and mechanisms. Arch Biochem Biophys 433:176–192

    Article  CAS  Google Scholar 

  • Tamer AÜ, Aragno M (1980) Isolement, caractérisation et essai d’identification de bactéries capables d’utiliser l’oxalate comme seule source de carbone et d’énergie. Bull la Société Neuchâteloise des Sci Nat 103:91–104

    Google Scholar 

  • Turroni S, Bendazzoli C, Dipalo SCF, Candela M, Vitali B, Gotti R, Brigidi P (2010) Oxalate-degrading activity in Bifidobacterium animalis subsp. lactis: impact of acidic conditions on the transcriptional levels of the oxalyl coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes. Appl Environ Microbiol 76:5609–5620

    Article  CAS  Google Scholar 

  • Verrecchia EP (1990) Litho-diagenetic implications of the calcium oxalate-carbonate biogeochemical cycle in semiarid Calcretes, Nazareth, Israel. Geomicrobiol J 8:87–99

    Article  CAS  Google Scholar 

  • Verrecchia E, Dumont J-L, Verrecchia KE (1993) Role of calcium oxalate biomineralization by fungi in the formation of calcretes: a case study from Nazareth, Israel. J Sediment Res 63:1000–1006

    CAS  Google Scholar 

  • Verrecchia E, Braissant O, Cailleau G (2006) The oxalate-carbonate pathway in soil carbon storage: the role of fungi and oxalotrophic bacteria. Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, pp 289–310

    Chapter  Google Scholar 

  • Zaitsev GM, Tsitko IV, Rainey FA, Trotsenko YA, Uotila JS, Stackebrandt E, Salkinoja-Salonen MS (1998) New aerobic ammonium-dependent obligately oxalotrophic bacteria: description of Ammoniphilus oxalaticus gen. nov., sp. nov. and Ammoniphilus oxalivorans gen. nov., sp. nov. Int J Syst Bacteriol 48:151–163

    Article  CAS  Google Scholar 

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  1. Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, 2000, Neuchâtel, Switzerland

    Vincent Hervé, Thomas Junier, Saskia Bindschedler & Pilar Junier

  2. Laboratory of Biogeosciences, Institute of Earth Sciences, University of Lausanne, Geopolis, 1015, Lausanne, Switzerland

    Vincent Hervé & Eric Verrecchia

  3. Vital-IT Group, Swiss Institute of Bioinformatics, Genopode, 1015, Lausanne, Switzerland

    Thomas Junier

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  1. Vincent Hervé
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  2. Thomas Junier
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  4. Eric Verrecchia
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Correspondence to Pilar Junier.

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Hervé, V., Junier, T., Bindschedler, S. et al. Diversity and ecology of oxalotrophic bacteria. World J Microbiol Biotechnol 32, 28 (2016). https://doi.org/10.1007/s11274-015-1982-3

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