Microbial Ecology

, Volume 73, Issue 2, pp 296–309 | Cite as

Phylotype Dynamics of Bacterial P Utilization Genes in Microbialites and Bacterioplankton of a Monomictic Endorheic Lake

  • Patricia M. Valdespino-Castillo
  • Rocío J. Alcántara-Hernández
  • Martín Merino-Ibarra
  • Javier Alcocer
  • Miroslav Macek
  • Octavio A. Moreno-Guillén
  • Luisa I. Falcón
Microbiology of Aquatic Systems


Microbes can modulate ecosystem function since they harbor a vast genetic potential for biogeochemical cycling. The spatial and temporal dynamics of this genetic diversity should be acknowledged to establish a link between ecosystem function and community structure. In this study, we analyzed the genetic diversity of bacterial phosphorus utilization genes in two microbial assemblages, microbialites and bacterioplankton of Lake Alchichica, a semiclosed (i.e., endorheic) system with marked seasonality that varies in nutrient conditions, temperature, dissolved oxygen, and water column stability. We focused on dissolved organic phosphorus (DOP) utilization gene dynamics during contrasting mixing and stratification periods. Bacterial alkaline phosphatases (phoX and phoD) and alkaline beta-propeller phytases (bpp) were surveyed. DOP utilization genes showed different dynamics evidenced by a marked change within an intra-annual period and a differential circadian pattern of expression. Although Lake Alchichica is a semiclosed system, this dynamic turnover of phylotypes (from lake circulation to stratification) points to a different potential of DOP utilization by the microbial communities within periods. DOP utilization gene dynamics was different among genetic markers and among assemblages (microbialite vs. bacterioplankton). As estimated by the system’s P mass balance, P inputs and outputs were similar in magnitude (difference was <10 %). A theoretical estimation of water column P monoesters was used to calculate the potential P fraction that can be remineralized on an annual basis. Overall, bacterial groups including Proteobacteria (Alpha and Gamma) and Bacteroidetes seem to be key participants in DOP utilization responses.


Extracellular enzymes DOP utilization Phytase P turnover Phylotype seasonality Microbial functional diversity 

Supplementary material

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  1. 1.
    Kolowith LC, Ingall ED, Benner R (2001) Composition and cycling of marine organic phosphorus. Limnol Oceanogr 46:309–320CrossRefGoogle Scholar
  2. 2.
    Björkman KM, Karl DM (2003) Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol Oceanogr 48(3):1049–1057CrossRefGoogle Scholar
  3. 3.
    Dyhrman ST, Ammerman JW, Van Mooy BAS (2007) Microbes and the marine phosphorus cycle. Oceanography 20:110–116CrossRefGoogle Scholar
  4. 4.
    White AE, Watkins-Brandt KS, Engle MA, Burkhardt B, Paytan A (2012) Characterization of the rate and temperature sensitivities of bacterial remineralization of dissolved organic phosphorus compounds by natural populations. Front Microbiol 3:276PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Biddanda B, Opsahl S, Benner R (1994) Plankton respiration and carbon flux through bacterioplankton on the Louisiana shelf. Limnol Oceanogr 39:1259–1275CrossRefGoogle Scholar
  6. 6.
    del Giorgio PA, Cole JJ, Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–151CrossRefGoogle Scholar
  7. 7.
    Benitez-Nelson CR, Buesseler KO (1999) Variability of inorganic and organic phosphorus turnover rates in the coastal ocean. Nature 6727:502–505CrossRefGoogle Scholar
  8. 8.
    Cotner JB, Wetzel RG (1992) Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton. Limnol Oceanogr 37(2):232–43CrossRefGoogle Scholar
  9. 9.
    Štrojsová A, Vrba J, Nedoma J, Komárková J, Znachor P (2003) Seasonal study of extracellular phosphatase expression in the phytoplankton of a eutrophic reservoir. Eur J Phycol 38(4):295–306CrossRefGoogle Scholar
  10. 10.
    Sebastian M, Ammerman JW (2009) The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J 3:563–572PubMedCrossRefGoogle Scholar
  11. 11.
    Luo H, Bennera R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proc Natl Acad Sci U S A 106:21219–21223PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Oh BC, Chang BS, Park KH, Ha NC, Kim HK, Oh BH et al (2001) Calcium-dependent catalytic activity of a novel phytase from Bacillus amyloliquefaciens DS11. Biochemistry 40(32):9669–9676PubMedCrossRefGoogle Scholar
  13. 13.
    Suzumura M, Kamatani A (1995) Origin and distribution of inositol hexaphosphate in estuarine and coastal sediments. Limnol Oceanogr 40:1254–1261CrossRefGoogle Scholar
  14. 14.
    Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME J 1(4):321–330PubMedGoogle Scholar
  15. 15.
    Huang H, Shi P, Wang Y, Luo H, Shao N, Wang G et al (2009) Diversity of beta-propeller phytase genes in the intestinal contents of grass carp provides insight into the release of major phosphorus from phytate in nature. Appl Environ Microbiol 75(6):1508–1516PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Cheng C, Lim BL (2006) Beta-propeller phytases in the aquatic environment. Arch Microbiol 185(1):1–13PubMedCrossRefGoogle Scholar
  17. 17.
    Jacobsen T, Slotfeldt-Ellingsen D (1983) Phytic acid and metal availability: a study of Ca and Cu binding. Cereal Chem 60(5):392–395Google Scholar
  18. 18.
    White AE (2009) New insights into bacterial acquisition of phosphorus in the surface ocean. PNAS 106(50):2013–2014CrossRefGoogle Scholar
  19. 19.
    Valdespino-Castillo PM, Alcántara-Hernández RJ, Alcocer J, Merino-Ibarra M, Macek M, Falcón LI (2014) Alkaline phosphatases in microbialites and bacterioplankton from Alchichica soda lake, Mexico. FEMS Microbiol Ecol 90(2):504–519PubMedGoogle Scholar
  20. 20.
    Giovannoni SJ, Vergin KL (2012) Seasonality in ocean microbial communities. Science 335:671–676PubMedCrossRefGoogle Scholar
  21. 21.
    Martínez J, Smith DC, Steward GF, Azam F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10:223–230. doi:10.3354/ame010223 CrossRefGoogle Scholar
  22. 22.
    Arnosti C, Durkin S, Jeffrey WH (2005) Patterns of extracellular enzyme activities among pelagic marine microbial communities: implications for cycling of dissolved organic carbon. Aquat Microb Ecol 38(2):135–145CrossRefGoogle Scholar
  23. 23.
    Vilaclara G, Chávez M, Lugo A, González H, Gaytán M (1993) Comparative description basic chemistry of crater-lakes in Puebla State, México. Verh Int Ver Theoret Angew Limnol 25:435–440Google Scholar
  24. 24.
    Armienta MA, Vilaclara G, De la Cruz-Reyna S, Ramos S, Ceniceros N, Cruz O, Aguayo A, Arcega-Cabrera F (2008) Water chemistry of lakes related to active and inactive Mexican volcanoes. J Volcanol Geoth Res 178(2):249–258CrossRefGoogle Scholar
  25. 25.
    Kazmierczak J, Kempe S, Kremer B, Lopez-Garcia P, Moreira D, Tavera R (2010) Hydrochemistry and microbialites of the alkaline crater lake Alchichica, Mexico. Facies 57:543–570CrossRefGoogle Scholar
  26. 26.
    Ramírez-Olvera MA, Alcocer J, Merino-Ibarra M, Lugo A (2009) Nutrient limitation in a tropical saline lake: a microcosm experiment. Hydrobiologia 626:5–13CrossRefGoogle Scholar
  27. 27.
    Ardiles V, Alcocer J, Vilaclara G, Oseguera LA, Velasco L (2012) Diatom fluxes in a tropical, oligotrophic lake dominated by large-sized phytoplankton. Hydrobiologia 679(1):77–90CrossRefGoogle Scholar
  28. 28.
    Lugo A, Alcocer J, Sanchez M, Escobar E (1998) Littoral protozoan assemblages from two Mexican hyposaline lakes. Hydrobiologia 381:9–13CrossRefGoogle Scholar
  29. 29.
    Alcocer J, Lugo A, Escobar E, Sánchez MR, Vilaclara G (2000) Water column stratification and its implications in the tropical warm monomictic lake Alchichica, Puebla, Mexico. Verh Int Ver Theoret Angew Limnol 27:3168–3169Google Scholar
  30. 30.
    Macek M, Alcocer J, Lugo-Vázquez A, Martínez-Pérez ME, Peralta Soriano L, Vilaclara Fatjó G (2009) Long term picoplankton dynamics in a warm-monomictic, tropical high altitude lake. J Limnol 68(2):183–192CrossRefGoogle Scholar
  31. 31.
    Hernández-Avilés JS, Macek M, Alcocer J, Lopez-Trejo B, Merino-Ibarra M (2010) Prokaryotic picoplankton dynamics in a warm-monomictic saline lake: temporal and spatial variation in structure and composition. J Plankton Res 32:1301–1314CrossRefGoogle Scholar
  32. 32.
    Centeno CM, Legendre P, Beltrán Y, Alcántara-Hernández RJ, Lidström UE, Ashby MN, Falcón LI (2012) Microbialite genetic diversity and composition relate to environmental variables. FEMS Microbiol Ecol 82(3):724–735PubMedCrossRefGoogle Scholar
  33. 33.
    Falcón LI, Escobar-Briones E, Romero D (2002) Nitrogen fixation patterns displayed by cyanobacterial consortia in Alchichica crater-lake, Mexico. Hydrobiologia 467(1–3):71–78CrossRefGoogle Scholar
  34. 34.
    Beltrán Y, Centeno CM, García-Oliva F, Legendre P, Falcón LI (2012) N2 fixation rates and associated diversity (nifH) of microbialite and mat-forming consortia from different aquatic environments in Mexico. Aquat Microb Ecol 67(1):15–24CrossRefGoogle Scholar
  35. 35.
    Grasshoff K, Kremling K, Ehrhardt M (1983) Methods of seawater analysis. Verlag Chemie, WeinheimGoogle Scholar
  36. 36.
    Kirkwood DS (1994) Sanplus segmented flow analyzer and its applications. Seawater analysis. Skalar, AmsterdamGoogle Scholar
  37. 37.
    Valderrama JC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar Chem 10:109–122CrossRefGoogle Scholar
  38. 38.
    Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322PubMedPubMedCentralGoogle Scholar
  39. 39.
    Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71CrossRefGoogle Scholar
  40. 40.
    Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A et al (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fert Soils 49(6):661–672CrossRefGoogle Scholar
  41. 41.
    Iwai S, Chai B, Jesus EDC, Penton CR, Lee TK, Cole JR, Tiedje JM (2011) Gene-targeted metagenomics (GT Metagenomics) to explore the extensive diversity of genes of interest in microbial communities. In: De Bruijn FJ (ed) Handbook of molecular microbial ecology I: metagenomics and complementary approaches. Wiley, Hoboken, pp 235–243CrossRefGoogle Scholar
  42. 42.
    Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321PubMedCrossRefGoogle Scholar
  43. 43.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedCrossRefGoogle Scholar
  45. 45.
    Geer LY, Marchler-Bauer A, Geer RC, Han L, He J, He S, Liu C, Shi W, Bryant SH (2010) The NCBI BioSystems database. Nucleic Acids Res 38(Database issue):D492–D496PubMedCrossRefGoogle Scholar
  46. 46.
    Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Chou PY, Fasman GD (1974) Conformational parameters for amino acids in helical, β-sheet, and random coil regions calculated from proteins. Biochemistry 13(2):211–222PubMedCrossRefGoogle Scholar
  48. 48.
    Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105–132PubMedCrossRefGoogle Scholar
  49. 49.
    Dworkin JE, Rose GD (1987) Hydrophobicity profiles revisited. In: Walsh KA (ed) Methods in protein sequence analysis. Humana, Clinton, pp 573–586Google Scholar
  50. 50.
    Baker D, Sali A (2001) Protein structure prediction and structural genomics. Science 294(5540):93–96PubMedCrossRefGoogle Scholar
  51. 51.
    Krystek SR Jr, Metzler WJ, Novotny J (2001) Hydrophobicity profiles for protein sequence analysis. Curr Protoc Protein Sci 00:2.2:2.2.1–2.2.13Google Scholar
  52. 52.
    García Martínez J (2010) Efectos climáticos sobre el agua subterránea y el lago Alchichica Puebla, México. Dissertation, Universidad Nacional Autónoma de MéxicoGoogle Scholar
  53. 53.
    Custodio E, Llamas MR (1983) Hidrología Subterránea Vol. II. Editorial Omega, MéxicoGoogle Scholar
  54. 54.
    Oliva MG, Lugo A, Alcocer J, Peralta L, Sánchez R (2001) Phytoplankton dynamics in a deep, tropical, hyposaline lake. Hydrobiologia 466:299–306CrossRefGoogle Scholar
  55. 55.
    Oliva MG, Lugo A, Alcocer J, Peralta L, Oseguera LA (2009) Planktonic bloomforming Nodularia in the saline Lake Alchichica, Mexico. Nat Resour Env Iss 15(1):22, http://digitalcommons.usu.edu/nrei/vol15/iss1/22 Google Scholar
  56. 56.
    Alcocer J, López-Anaya DP, Oseguera LA (2007) Dinámica del carbono orgánico particulado en un lago tropical profundo. In: Hernández de la Torre B, Gaxiola Castro G (ed) Carbono en ecosistemas acuáticos de México. INE, México, pp 239–247Google Scholar
  57. 57.
    Ramírez-Zierold JA, Merino-Ibarra M, Monroy-Ríos E, Olson M, Castillo FS, Gallegos ME, Vilaclara G (2010) Changing water, phosphorus and nitrogen budgets for Valle de Bravo reservoir, water supply for Mexico City Metropolitan Area. Lake Reserv Manag 26(1):23–34CrossRefGoogle Scholar
  58. 58.
    Oseguera LA, Alcocer J, Vilaclara G (2011) Relative importance of dust inputs and aquatic biological production as sources of lake sediments in an oligotrophic lake in a semi-arid area. Earth Surf Processes 36(3):419–426CrossRefGoogle Scholar
  59. 59.
    Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R et al (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43(Database issue):D213–D221PubMedCrossRefGoogle Scholar
  60. 60.
    Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230PubMedCrossRefGoogle Scholar
  61. 61.
    Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY et al (2014) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(Database issue):D222–D226PubMedPubMedCentralGoogle Scholar
  62. 62.
    Ponting CP (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci 5(11):2353–2357PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Hiroaki H, Ago T, Ito T, Sumimoto H, Kohda D (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat Struct Biol 8(6):526–530. doi:10.1038/88591.PMID11373621 PubMedCrossRefGoogle Scholar
  64. 64.
    Ago T, Kuribayashi F, Hiroaki H, Takeya R, Ito T, Kohda D, Sumimoto H (2003) Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc Natl Acad Sci U S A 100(8):4474–4479PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Wishart MJ, Taylor GS, Dixon JE (2001) Phoxy lipids: revealing PX domains as phosphoinositide binding modules. Cell 105(7):817–820. doi:10.1016/S0092-8674(01)00414-7.PMID11439176 PubMedCrossRefGoogle Scholar
  66. 66.
    Márquez JA, Hasenbein S, Koch B, Fieulaine S, Nessler S, Russell RB et al (2002) Structure of the full-length HPr kinase/phosphatase from Staphylococcus xylosus at 1.95 Å resolution: mimicking the product/substrate of the phospho transfer reactions. Proc Natl Acad Sci U S A 99(6):3458–3463PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Sebastián M, Gasol JM (2013) Heterogeneity in the nutrient limitation of different bacterioplankton groups in the Eastern Mediterranean Sea. ISME J 7(8):1665–1668PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Jorquera M, Martínez O, Maruyama F, Marschner P, de la Luz Mora M (2008) Current and future biotechnological applications of bacterial phytases and phytase-producing bacteria. Microbes Environ 23(3):182–191PubMedCrossRefGoogle Scholar
  69. 69.
    Goodacrea NF, Gerloffb DL, Uetzc P (2013) Protein domains of unknown function are essential in bacteria. mBio 5(1):e00744–13Google Scholar
  70. 70.
    Read EK, Ivancic M, Hanson P, Cade-Menun BJ, McMahon KD (2014) Phosphorus speciation in a eutrophic lake by 31 P NMR spectroscopy. Water Res 62:229–240PubMedCrossRefGoogle Scholar
  71. 71.
    Cotner J, Wetzel RG (1992) Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton. Limnol Oceanogr 37(2):232–243CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Patricia M. Valdespino-Castillo
    • 1
    • 2
  • Rocío J. Alcántara-Hernández
    • 3
  • Martín Merino-Ibarra
    • 4
  • Javier Alcocer
    • 5
  • Miroslav Macek
    • 5
    • 6
  • Octavio A. Moreno-Guillén
    • 1
    • 7
  • Luisa I. Falcón
    • 1
  1. 1.Laboratorio de Ecología Bacteriana, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  2. 2.Secretaría de Ciencia, Tecnología e Innovación del Distrito Federal-Centro Latino-Americano de FísicaMexico CityMexico
  3. 3.Instituto de GeologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  4. 4.Unidad Académica de Ecología y Biodiversidad Acuática, Instituto de Ciencias del Mar y LimnologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  5. 5.Proyecto de Investigación en Limnología Tropical, FES IztacalaUNAMTlalnepantlaMexico
  6. 6.Biology Centre v. v. i., Institute of HydrobiologyAcademy of Sciences of the Czech RepublicČeské BudějoviceCzech Republic
  7. 7.Posgrado en Ciencias BiológicasUniversidad Nacional Autónoma de MéxicoMexico CityMexico

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