Advertisement

Annals of Microbiology

, Volume 65, Issue 1, pp 1–13 | Cite as

Composition of supralittoral sediments bacterial communities in a Mediterranean island

  • Giovanni Bacci
  • Ettore Pagoto
  • Maurizio Passaponti
  • Pietro Vannocci
  • Alberto Ugolini
  • Alessio MengoniEmail author
Original Article

Abstract

Marine coasts represent highly dynamic ecosystems, with sandy beaches being one of the most heterogeneous. Despite the key importance of sandy beaches as transition ecosystems between sea and land, very few studies on the microbiological composition of beach sediments have been performed. To provide a first description of microbial composition of supralittoral sediments, we investigated the composition of bacterial communities of three sandy beaches, at Favignana Island, Italy, using metagenetic approaches (Terminal-Restriction Fragment Length Polymorphism, sequencing of 16S rRNA genes by Illumina-Solexa technology, functional genes detection, and quantitative Real-Time PCR). Results showed that the investigated beaches are harboring a rich bacterial diversity, mainly composed by members of classes Alphaproteobacteria, Gammaproteobacteria, Flavobacteria and Actinobacteria. The metagenetic analysis showed profiles of decreasing beta diversity and increasing richness, as well as a differentiation of communities, along the sea-to-land axis. In particular, members of Firmicutes and Proteobacteria displayed contrasting profiles of relative abundance (to decrease and to increase, respectively) along the sea-to-land axis of the beach. Finally, a search for the presence of genes related to the nitrogen and carbon biogeochemical cycle (nifH, nosZ, pmoA/amoA) detected the presence of ammonia monoxygenase sequences (amoA) only, suggesting the presence of bacterial ammonia oxidation to some extent, probably due to members of Nitrospira, but with the lack of nitrogen fixation and denitrification.

Keywords

Supralittoral zone Sandy beaches Bacterial communities T-RFLP 16S rRNA gene Metabarcoding 

Notes

Acknowledgments

We are grateful to the Marine Protected Area “Isole Egadi” for authorization to obtain samplings. This work was supported by intramural funding (Fondo di Ateneo, ex 60%) of the University of Florence to AU and AM.

Supplementary material

13213_2014_829_MOESM1_ESM.pdf (1.8 mb)
Figure S1 Flowchart of the resampling procedure (PDF 1806 kb)
13213_2014_829_MOESM2_ESM.pdf (57 kb)
Figure S2 Boxplots of random taxonomic attribution obtained with resample and observed differences. The observed differences were plotted as a red point and or blue triangle. See material and methods for details (PDF 56 kb)
13213_2014_829_MOESM3_ESM.pdf (141 kb)
Figure S3 Rarefaction analysis on different taxonomic levels. a) Phylum; b) Order; c) Class; d) Family. Each curve was rarefied using the minimum richness value from one of the tree samples. The analysis shows that an exhaustive overview of the total biodiversity could only be achieved considering less specific taxonomic levels as the order or family levels (PDF 140 kb)

References

  1. Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-End illumina reads. Appl Environ Microbiol 77:3846–3852CrossRefPubMedCentralPubMedGoogle Scholar
  2. Bonadonna L, Cataldo C, Semproni M, Briancesco R (2003) Sanitary quality of marine sediments and sands from an Italian beach. New Microbiol 26:199–206PubMedGoogle Scholar
  3. Bourne DG, McDonald IR, Murrell JC (2001) Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl Environ Microbiol 67:3802–3809CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bowles JE (1988) Engineering properties of soils and their measurement. Mc Graw Hill International Edition, SingaporeGoogle Scholar
  5. Brown AC, McLachlan A (2002) Sandy shore ecosystems and the threats facing them: some predictions for the year 2025. Environ Conserv 29:62–77CrossRefGoogle Scholar
  6. Bull AT, Stach JEM, Ward AC, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges, future directions. Antonie Van Leeuwenhoek 87:65–79CrossRefGoogle Scholar
  7. Cui Z, Lai Q, Dong C, Shao Z (2008) Biodiversity of polycyclic aromatic hydrocarbon-degrading bacteria from deep sea sediments of the Middle Atlantic Ridge. Environ Microbiol 10:2138–2149CrossRefPubMedCentralPubMedGoogle Scholar
  8. Dalmastri C, Chiarini L, Cantale C, Bevivino A, Tabacchioni S (1999) Soil type and maize cultivar affect the genetic diversity of maize root-associated Burkholderia cepacia populations. Microb Ecol 38:273–284CrossRefPubMedGoogle Scholar
  9. Dohrmann AB, Kuting M, Junemann S, Jaenicke S, Schluter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. ISME J 7:37–49CrossRefPubMedCentralPubMedGoogle Scholar
  10. Excoffier L, Laval G, Schneider S (2007) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinforma 1:47–50Google Scholar
  11. Excoffier L, Smouse PE, Quattro M (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  12. Figueira D, Barata M (2007) Marine fungi from two sandy beaches in Portugal. Mycologia 99:20–23CrossRefPubMedGoogle Scholar
  13. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Micro 9:403–413Google Scholar
  14. Gerber GK, Onderdonk AB, Bry L (2012) Inferring dynamic signatures of microbes in complex host ecosystems. PLoS Comput Biol 8:e1002624CrossRefPubMedCentralPubMedGoogle Scholar
  15. Giuntini E, Bazzicalupo M, Castaldini M, Fabiani A, Miclaus N, Piccolo R, Ranalli G, Santomassimo F, Zanobini S, Mengoni A (2006) Genetic diversity of dinitrogen-fixing bacterial communities in soil amended with olive husks. Ann Microbiol 56:83–88CrossRefGoogle Scholar
  16. Glavin DP, Cleaves HJ, Schubert M, Aubrey A, Bada JL (2004) New method for estimating bacterial cell abundances in natural samples by use of sublimation. Appl Environ Microbiol 70:5923–5928CrossRefPubMedCentralPubMedGoogle Scholar
  17. Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, MacPhee R, Reid G (2010) Microbiome profiling by illumina sequencing of combinatorial sequence-tagged PCR products. PLoS ONE 5:e15406CrossRefPubMedCentralPubMedGoogle Scholar
  18. Gobet A, Böer SI, Huse SM, Van Beusekom JEE, Quince C, Sogin ML, Boetius A, Ramette A (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6:542–553CrossRefPubMedCentralPubMedGoogle Scholar
  19. Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: How biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450CrossRefPubMedGoogle Scholar
  20. Green-Garcìa AM, Engel AS (2012) Bacterial diversity of siliciclastic sediments in a Thalassia testudinum meadow and the implications for Lucinisca nassula chemosymbiosis. Estuar Coast Shelf Sci 112:153–161CrossRefGoogle Scholar
  21. Haaijer SCM, Ji K, Van Niftrik L, Hoischen A, Speth DR, Jetten MSM, Sinninghe Damsté JS, Op Den Camp HJM (2013) A novel marine nitrite-oxidizing Nitrospira species from Dutch coastal North Sea water. Front Microbiol 4:60CrossRefPubMedCentralPubMedGoogle Scholar
  22. Hallberg K, Hedrich S, Johnson D (2011) Acidiferrobacter thiooxydans gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae. Extremophiles 15:271–279CrossRefPubMedGoogle Scholar
  23. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 41:9Google Scholar
  24. Head KH (1984) Manual of soil laboratory testing. Vol 1: soil classification and compaction tests. ELE International Ltd, LondonGoogle Scholar
  25. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11CrossRefPubMedGoogle Scholar
  26. Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208CrossRefPubMedGoogle Scholar
  27. Horz H-P, Rich V, Avrahami S, Bohannan BJM (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl Environ Microbiol 71:2642–2652CrossRefPubMedCentralPubMedGoogle Scholar
  28. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255CrossRefPubMedCentralPubMedGoogle Scholar
  29. Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386CrossRefPubMedCentralPubMedGoogle Scholar
  30. Ivanova EP, Mikhailov VV (2001) A new family, Alteromonadaceae fam. nov., including marine Proteobacteria of the genera Alteromonas, Pseudoalteromonas, Idiomarina, and Colwellia. Microbiology 70:10–17CrossRefGoogle Scholar
  31. Jin HM, Lee HJ, Kim JM, Park MS, Lee K, Jeon CO (2011) Litorimicrobium taeanense gen. nov., sp. nov., isolated from a sandy beach. Int J Syst Evol Bacteriol 61:1392–1396CrossRefGoogle Scholar
  32. Lee K-B, Liu C-T, Anzai Y, Kim H, Aono T, Oyaizu H (2005) The hierarchical system of the Alphaproteobacteria: description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. Int J Syst Evol Bacteriol 55:1907–1919CrossRefGoogle Scholar
  33. Ludwig B, Geisseler D, Michel K, Joergensen RG, Schulz E, Merbach I, Raupp J, Rauber R, Hu K, Niu L, Liu X (2011) Effects of fertilization and soil management on crop yields and carbon stabilization in soils. A review. Agron Sustain Dev 31:361–372CrossRefGoogle Scholar
  34. McLachlan A, Brown A (2006) The ecology of sandy shores. Elsevier, AmsterdamGoogle Scholar
  35. Mengoni A, Bazzicalupo M (2002) The statistical treatment of data and the analysis of MOlecular VAriance (AMOVA) in molecular microbial ecology. Ann Microbiol 52:95–101Google Scholar
  36. Mengoni A, Pini F, Huang L-N, Shu W-S, Bazzicalupo M (2009) Plant-by-plant variations of bacterial communities associated with leaves of the nickel-hyperaccumulator Alyssum bertolonii Desv. Microb Ecol 58:660–667CrossRefPubMedGoogle Scholar
  37. Mengoni A, Tatti E, Decorosi F, Viti C, Bazzicalupo M, Giovannetti L (2005) Comparison of 16S rRNA and 16S rDNA T-RFLP approaches to study bacterial communities in soil microcosms treated with chromate as perturbing agent. Microb Ecol 50:375–384CrossRefPubMedGoogle Scholar
  38. Misic C, Fabiano M (2005) Enzymatic activity on sandy beaches of the Ligurian Sea (NW Mediterranean). Microb Ecol 49:513–522CrossRefPubMedGoogle Scholar
  39. Mizrahi-Man O, Davenport ER, Gilad Y (2013) Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs. PLoS ONE 8:e53608CrossRefPubMedCentralPubMedGoogle Scholar
  40. Mudryk ZJ (2005) Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach. Mar Pollut Bull 50:80–86CrossRefPubMedGoogle Scholar
  41. Musat N, Werner U, Knittel K, Kolb S, Dodenhof T, van Beusekom JEE, de Beer D, Dubilier N, Amann R (2006) Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Rømø Basin, Wadden Sea. Syst Appl Microbiol 29:333–348CrossRefPubMedGoogle Scholar
  42. Pastorelli R, Landi S, Trabelsi D, Piccolo R, Mengoni A, Bazzicalupo M, Pagliai M (2011) Effects of soil management on structure and activity of denitrifying bacterial communities. Appl Soil Ecol 49:49–58CrossRefGoogle Scholar
  43. Pini F, Frascella A, Santopolo L, Bazzicalupo M, Biondi E, Scotti C, Mengoni A (2012) Exploring the plant-associated bacterial communities in Medicago sativa L. BMC Microbiol 12:78CrossRefPubMedGoogle Scholar
  44. Pukall R, Buntefuss D, Fruhling A, Rohde M, Kroppenstedt RM, Burghardt J, Lebaron P, Bernard L, Stackebrandt E (1999) Sulfitobacter mediterraneus sp. nov., a new sulfite-oxidizing member of the α-Proteobacteria. Int J Syst Bacteriol 49:513–519CrossRefPubMedGoogle Scholar
  45. Rich JJ, Heichen RS, Bottomley PJ, Cromack K, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982CrossRefPubMedCentralPubMedGoogle Scholar
  46. Rosano-Hernandez MC, Ramìrez-Saad H, Fernandez-Linares L (2012) Petroleum-influenced beach sediments of the Campeche bank, Mexico: diversity and bacterial community structure assessment. J Environ Manag 95:S325–S331CrossRefGoogle Scholar
  47. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcón LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The sorcerer II global ocean sampling expedition: Northwest Atlantic through eastern tropical pacific. PLoS Biol 5:0398–0431CrossRefGoogle Scholar
  48. Schlacher TA, Dugan J, Schoeman DS, Lastra M, Jones A, Scapini F, McLachlan A, Defeo O (2007) Sandy beaches at the brink. Divers Distrib 13:556–560CrossRefGoogle Scholar
  49. Schlacher TA, Schoeman DS, Dugan J, Lastra M, Jones A, Scapini F, McLachlan A (2008) Sandy beach ecosystems: key features, sampling issues, management challenges and climate change impacts. Mar Ecol-Evol Perspect 29:70–90CrossRefGoogle Scholar
  50. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92CrossRefPubMedCentralPubMedGoogle Scholar
  51. Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, Martiny JBH (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10:2200–2210CrossRefPubMedGoogle Scholar
  52. Simmons SL, Bazylinski DA, Edwards KJ (2007) Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ Microbiol 9:2162–2174CrossRefPubMedGoogle Scholar
  53. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103:12115–12120CrossRefPubMedCentralPubMedGoogle Scholar
  54. Sorokin DY, Tourova TP, Muyzer G, Kuenen GJ (2008) Thiohalospira halophila gen. nov., sp. nov. and Thiohalospira alkaliphila sp. nov., novel obligately chemolithoautotrophic, halophilic, sulfur-oxidizing gammaproteobacteria from hypersaline habitats. Int J Syst Evol Microbiol 58:1685–1692CrossRefPubMedGoogle Scholar
  55. Tabacchioni S, Chiarini L, Bevivino A, Cantale C, Dalmastri C (2000) Bias caused by using different isolation media for assessing the genetic diversity of a natural microbial population. Microb Ecol 40:169–176PubMedGoogle Scholar
  56. Teplinskaia NG (1978) Microflora of the sandy beaches of the Odessa shoreline possessing lipolytic activity. Mikrobiol Z 40:709–715Google Scholar
  57. Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES, Sorokin DY (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57:2387–2398CrossRefPubMedGoogle Scholar
  58. Trabelsi D, Mengoni A, Aouani ME, Mhamdi R, Bazzicalupo M (2009) Genetic diversity and salt tolerance of bacterial communities from two Tunisian soils. Ann Microbiol 59:25–32CrossRefGoogle Scholar
  59. Ugolini A, Ungherese G (2012) Sandhoppers as bioindicators of anthropogenic influence on Mediterranean sandy beaches. In: Stambler N (ed) Life in the Mediterranean Sea: a look at habitat changes. Nova Science Publisher, New York, pp 413–443Google Scholar
  60. Ugolini A, Ungherese G, Somigli S, Galanti G, Baroni D, Borghini F, Cipriani N, Nebbiai M, Passaponti M, Focardi S (2008) The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches. Mar Environ Res 65:349–357CrossRefPubMedGoogle Scholar
  61. Wackett LP (2013) Bacteria in sand. Environ Microbiol 15:2144–2145CrossRefPubMedGoogle Scholar
  62. Widmer F, Shaffer BT, Porteous LA, Seidler RJ (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in Oregon Cascade Mountain Range. Appl Environ Microbiol 65:374–380PubMedCentralPubMedGoogle Scholar
  63. Zweifel UL, Hagstrom A (1995) Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (ghosts). Appl Environ Microbiol 61:2180–2185PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2014

Authors and Affiliations

  • Giovanni Bacci
    • 1
    • 2
  • Ettore Pagoto
    • 1
  • Maurizio Passaponti
    • 3
  • Pietro Vannocci
    • 4
  • Alberto Ugolini
    • 1
  • Alessio Mengoni
    • 1
    Email author
  1. 1.Department of BiologyUniversity of FlorenceSesto FiorentinoItaly
  2. 2.Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Centro di Ricerca per lo Studio delle Relazioni tra Pianta e Suolo (CRA-RPS)RomeItaly
  3. 3.Department of ChemistryUniversity of FlorenceSesto FiorentinoItaly
  4. 4.Department of Earth ScienceUniversity of FlorenceFlorenceItaly

Personalised recommendations