Prof. Marla Trindade

DST/NRF SARChI, Research Chair in Microbial Genomics

Director of IMBM: Institute for Microbial Biotechnology & Metagenomics

Research Projects:

My research interests lie in the microbial ecology of various environments, including thermophilic, psychrophilic, acidophilic, haloalkalophilic, marine and freshwater lakes. I am also investigating the microbial communities associated with important South African plants, including sorghum and fynbos. The understanding of microorganisms in their environment creates a natural link with biotechnology. Processes, mechanisms and products associated with microbial survival in an environment can be exploited for white, green and blue biotechnology. I therefore have several diverse interests in the application of microorganisms in biotechnology.

Contact: ituffin@uwc.ac.za, prof.marlatt@gmail.com

Publications:

BOOK CHAPTERS

  1. Cowan D, Tuffin M, Robb F. 2010. ‘‘Sequence First, Ask Questions Later’’: The Impact of Next Generation-Omics on the Discovery of Novel Microbial and Lipid Hydrocarbon Metabolism. In: Timmis, Kenneth N. (Ed.) Handbook of Hydrocarbon and Lipid Microbiology, Springer Heidelberg, Vol 4, pp. 3367-3374.
  2. Casanueva A, Tuffin M, Cowan DA. 2010. Nanoarchaeota: Physiology, Genomics and Phylogeny, Chapter 7 In S. Kato (ed) “Archaea: Structure, Habitats and Ecological Significance, Nova Publishers. pp. 163-174.
  3. Meiring, T. L., Mulako, I., Tuffin, M., Meyer, Q., Cowan, DA. 2010. Retrieval of Full Length Functional Genes using Subtractive Hybridization Magnetic Bead Capture. Ch. 20 In: Metagenomics: Methods and Protocols, Vol. 668 of Methods in Molecular Biology. W. Streit and R. Daniel (Ed.): Humana Press Inc. Totowa NJ, USA. pp. 287-298.
  4. Meiring, T., Bauer, R., Scheepers, I., Ohlhoff, C., Tuffin, M., Cowan, D. 2011. Metagenomics and beyond: current approaches and integration with complementary technologies. Ch. In Metagenomics: Current innovations and future trends. Marco, D., ed. Caister Acad. Press, Publ. pp. 1-26.
  5. Taylor, MP, Van Zyl, L, Tuffin, M, Cowan, DA. 2012. Extremophiles and biotechnology: How far have we come? Ch 1. In Extremophiles: Microbiology and Biotechnology. Antinori, R., Ed.  Caister Academic Press. pp. 1-24.
  6. Mutondo, M., Huddy, R., Bauer, R., Tuffin, M., Cowan, D. 2013. Metagenomic gene discovery. Ch. 15 In Metagenomics and its applications in agriculture, biomedicine and Environmental studies. RW Li, Ed. pp. 287-320.
  7. Kirby, B., Le Roess-Hill, M., Cary, S., Burton, S., Tuffin, M., Cowan, D. 2011. Actinobacterial diversity associated with Antarctic Dry Valley mineral soils. Ch. 13 In Handbook of Molecular Microbial Ecology II: Metagenomics in different habitats. Frans de Bruijn, Ed., John Wiley & Sons, Inc., Hoboken, New Jersey. pp. 123-133.
  8. Taylor, M., Ramond, J-B., Tuffin, S., Burton, S., Eley, K., Cowan, D. 2011. Mechanisms and Applications of Microbial Stress Tolerance. Ch. 8 In: Microbial stress tolerance for biofuels. Liu, Z L., Ed., Springer Berlin Heidelberg. pp. 177-208.
  9. Kirby, BM, Easton, S, Tuffin, IM, Cowan, DA. 2012. Bacterial Diversity in Polar Habitats. Ch. 1 In: Polar Microbiology: Life in a deep freeze. Miller, RV, Whyte, LG., Eds. ASM Press. pp. 3-31.
  10. Kirby, BM, Barnard, D, Tuffin, IM, Cowan, DA. 2011. Ecological distribution of microorganisms in terrestrial, psychrophilic habitats. In: Extremophiles Handbook. Horikoshi, K., Ed., Springer. pp. 839-863.
  11. Cowan, D., Tuffin, M., Mulako, I., Cass, J. 2012. Terrestrial Hydrothermal Environments. Ch. 12 In: Life at Extremes: Environments, Organisms, and Strategies for Survival, Bell, E., Ed., CABI Press. pp. 219-241.
  12. MP Taylor, R Bauer, S Mackay, M Tuffin, DA Cowan. 2012. Extremophiles and their application to biofuel research. Ch. 9 In: Sustainable Resources and Biotechnological Implications. OV Singh, Ed; Wiley. pp. 233-265. DOI: 10.1002/9781118394144.
  13. Smart M, Huddy R, Cowan D, Trindade M. 2017. Liquid Phase Multiplex High-Throughput Screening of Metagenomic Libraries Using p-Nitrophenyl-Linked Substrates for Accessory Lignocellulosic Enzymes. In: Streit W., Daniel R. (eds) Metagenomics, Methods and Protocols, Methods in Molecular Biology, vol 1539. Springer Science+Business Media, Humana Press, New York, NY. pp 219-228.
  14. Williams W, Trindade M. 2017. Metagenomics for the Discovery of Novel Biosurfactants. In: Charles T., Liles M., Sessitsch A. (eds) Functional Metagenomics: Tools and Applications. Springer, Cham. Pp 95-117.
  15. Mhlongo J, Beukes D, Trindade M. 2018. Endosymbiotic Bacteria Isolated from Algoa and Kalk Bay, South Africa, as Source of Antimicrobial Compounds. In: Ramasami P., Gupta Bhowon M., Jhaumeer Laulloo S., Li Kam Wah H. (eds) Emerging Trends in Chemical Sciences. ICPAC 2016. Springer, Cham. Pp 355-364.
  16. Cowan DA, Adriaenssens E, Pieter De Maayer P, Lebre P, Makhalanyane TP, Ramond J-B, Trindade IM, Valverde A, Vikram S. 2018. Metagenomics of Extreme Environments: Methods and Applications. Chapter X, in Advanced Techniques for Studying Microorganisms in Extreme Environments, E Yergeau, Ed. De Gruyter, Publ. In Press (ISBN 978-3-11-052578-6).

PAPERS

  1. Trindade, M., V. Abratt, S. Reid. 2003. Induction of sucrose-utilising genes from Bifidobacterium lactis by sucrose and raffinose. Applied and Environmental Microbiology. 69: 24-32.
  2. Tuffin, M., P. de Groot, S. Deane & D. Rawlings. 2004. Multiple sets of arsenic resistance genes are present within highly arsenic resistant industrial strains of the biomining bacterium, Acidithiobacillus caldus. International Congress Series. 1275: 165-172.
  3. Tuffin, M., P. de Groot, S. Deane & D. Rawlings. 2005. An unusual Tn21-like transposon containing an ars operon is present in highly arsenic resistant strains of the biomining bacterium Acidithiobacillus caldus. Microbiology. 151: 3027-3039.
  4. Tuffin, M., S. Hector, S. Deane & D. Rawlings. 2006. Resistance determinants of a highly arsenic resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank. Applied and Environmental Microbiology. 72: 2247-2253.
  5. Kotze, A., M. Tuffin, S. Deane & D. Rawlings. 2006. Isolation of the chromosomal arsenic resistance genes from Acidithiobacillus caldus and enhanced arsenic resistance on conjugal transfer of ars genes located on transposon TnAtcArs. Microbiology. 152: 3551–3560.
  6. Taylor, M., Tuffin, M., Burton, S., Eley, K., Cowan, D. 2008. Microbial responses to solvent and alcohol stress. Biotechnol. J. Nov;3(11):1388-97.
  7. Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA. 2009. Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol. 27:398-405.
  8. Tuffin, M., Anderson, A., Heath, C., Cowan, D. 2009. Metagenomic gene discovery: How far have we moved into novel sequence space? Biotechnology Journal. 4(12): 1671-1683.
  9. Cowan, D., Tuffin, M. 2009. Capturing global metabolism. Nature biotechnology. 27(12): 1132-1133.
  10. Staniland, S., Coppock, M., Tuffin, M., van Zyl, L., Roychoudhury, A. N., Cowan, D. 2010. Cobalt uptake and resistance to trace metals in Comamonas testosteroni isolated from a heavy-metal contaminated site in the Zambian Copperbelt. Geomicrobiology Journal. 27(8): 656 – 668.
  11. Musingarimi, W., Tuffin, M., Cowan, D. 2010. Characterisation of the Arsenic Resistance Genes in Bacillus sp. UWC Isolated from Maturing Fly Ash-Acid Mine Drainage Neutralized Solids. South African Journal of Science. 106: 59-63.
  12. Casanueva, A., Tuffin, M., Cary, C., Cowan, C. 2010. Molecular adaptations to psychrophily: the impact of “omic” technologies. Trends in Microbiology. 18: 374-381.
  13. Barnard, D. Casanueva, A., Tuffin, M., Cowan, D. 2010. Extremophiles in biofuel synthesis. Environmental Technology. 31(8): 871-888.
  14. Cowan, A., Pointing, S., Stevens, M., Cary, C., Stomeo, F., Tuffin, M. 2011. Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Microbiology. 34:307–311.
  15. Taylor, MP, Van Zyl, L, Tuffin, M, Leak, D., Cowan, DA. 2011. Genetic tool development underpins recent advances in thermophilic whole cell biocatalysts. Microbial Biotechnology. 4(4): 438–448.
  16. Nel, A., Tuffin, M., Sewell, T., Cowan, D. 2011. A unique aliphatic amidase from a psychrophiic and haloalkaliphilic Nesterenkonia isolate. Applied and Environmental Microbiology. 77(11): 3696-3702.
  17. Taylor, M., Mulako, I., Tuffin, M., Cowan, D. 2011. Understanding physiological responses to pre-treatment inhibitors in ethanologenic fermentations. Biotech J. 7 (9): 1169-1181.
  18. Rohr, LM, Mashaphu, N, Sheridan, C, Burton, SG, Tuffin, M., and Cowan, DA. 2011. Seasonal shifts of the microbial community structure in a winery waste-impacted wetland soil. Trans. Roy. Soc. SA. 66(1): 41-53.
  19. Khan, N., Tuffin, M., Stafford, W., Cary, C., Lacap, D., Pointing, S., Cowan, DA. 2011. Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biology, 34(11), 1657-1668.
  20. Cowan, DA, Sohm, JA, Makhalanyane, T, Capone, DG, Green, TGA and Cary, SC. Tuffin, M. 2011. Hypolithic communities: an important nitrogen source in Antarctic desert soils, Envir Microbiol. 3(5): 381-386.
  21. Hu XP, Heath C, Taylor MP, Tuffin M, Cowan DA. 2012. A novel, extremely alkaliphilic and cold-active esterase from Antarctic desert soil. Extremophiles 16(1):79-86.
  22. Stomeo, Francesca; Makhalanyane, Thulani; Valverde, Angel; Pointing, Stephen; Stevens, Mark; Cary, Stephen; Tuffin, Marla; Cowan, Don. 2012. Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiology Ecology. 82(2):326-40.
  23. Cowan, D., Chown, S., Convey, P., Tuffin, M., Hughes, K., Pointing, S., Vincent, W. 2011. Non-indigenous microorganisms in the Antarctic- assessing the risks. Trends Microbiol. 19(11):540–548.
  24. Meiring, T, Tuffin, M, Cowan, D. 2012. Genome sequence of temperate bacteriophage Psymv2 from Antarctic Dry Valley soil isolate Psychrobacter sp. MV2. Extremophiles. 16(5):715-726.
  25. Valverde, A., Tuffin, M., Cowan, D. 2012. Biogeography of bacterial communities in hot springs: a focus on the actinobacteria. Extremophiles. 16(4): 669-679.
  26. Makhalanyane, T., Valverde, A., Pointing, S., Tuffin, S., Cowan, D. 2013. Evidence of species recruitment and development of hot desert hypolithic communities. Environmental Microbiology Reports. 5(2): 219-224.
  27. Loftie-Eaton, W., Taylor, M., Horne, K., Tuffin, M., Burton, S., Cowan, D. 2013. Balancing redox cofactor generation and ATP synthesis: Key microaerobic responses in thermophilic fermentations. Biotechnology and Bioengineering. 110(4): 1057-1065.
  28. Stomeo, F., Valverde, A., Pointing, S., McKay, C., Warren-Rhodes, K., Tuffin, M., Seely, M., Cowan, D. 2013. Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert. Extremophiles. 17(2): 329-337.
  29. Gokul, J., Valverde, A., Tuffin, M., Cowan, D. 2013. Micro-eukaryotic diversity in hypolithons from Miers Valley, Antarctica. Biology. 2(1): 331-340.
  30. Ramond, JB., Welz, P., Tuffin, M., Burton, S., Cowan, D. 2013. Assessment of temporal and spatial evolution of bacterial communities in a biological sand filter mesocosm treating winery wastewater. Journal of Applied Microbiology. 115(1):9 1-101.
  31. Ramond, J-B., Tshabuse, F., Bopda, C., Cowan, D., Tuffin, M. 2013. Evidence of variability in the structure and recruitment of rhizospheric and endophytic bacteria communities associated with arable sweet sorghum (Sorghum bicolor (L) Moench). Plant and Soil. 372: 265-278.
  32. Ramond, JB., Welz, P., Tuffin, M., Burton, S., Cowan, D. 2013. Selection of diazotrophic bacterial communities in biological sand filter mesocosms used for the treatment of phenolic-laden wastewater. Microbial Ecology. DOI 10.1007/s00248-013-0258-4.
  33. Makhalanyane, T., Valverde, A., Tuffin, S., Cowan, D. 2013. Evidence for successional development in Antarctic hypolithic bacterial communities. ISME. 7: 2080-2090.
  34. Cowan, D., Rybicki, E., Tuffin, M., Valverde, A., Wingfield, M. 2013. Biodiversity: So Much More than Legs and Leaves. South African Journal of Science. 109: 8-15.
  35. Van Zyl, L., Taylor, M., Tuffin, M., Eley, K., Cowan, D. 2014. Engineering pyruvate decarboxylase-mediated ethanol production in the thermophilic host Geobacillus thermoglucosidasius. Applied Microbiology and Biotechnology. 98(3):1247-59.
  36. Aliyu, H., De Maayer, P., Rees, J., Tuffin, M., Cowan, D. 2014. Draft Genome Sequence of the Antarctic Polyextremophile Nesterenkonia sp. Strain AN1. Genome Announcements. 2(2): e00197-14.
  37. Ramond, J-B., Welz, P., Le Roes-Hill, M., Tuffin, M., Burton, S., Cowan, D. 2014. Selection of Clostridium spp. in biological sand filters neutralizing synthetic acid mine drainage. FEMS Microbiology Ecology. 87(3):678-90.
  38. van Zyl, L., Schubert, W-D., Tuffin, M., Cowan, C. 2014. Structure and Functional Characterization of a Pyruvate decarboxylase from Gluconacetobacter diazotrophicus. BMC Structural Biology. 14(21). doi:10.1186/s12900-014-0021-1.
  39. Zablocki O., van Zyl L., Adriaenssens E., Rubagotti, E., Tuffin, M., Cary, S., Cowan, D. 2014. Niche-dependent genetic diversity in Antarctic metaviromes. Bacteriophage. 4(4): e980125.
  40. Zablocki O., van Zyl L., Adriaenssens E., Rubagotti, E., Tuffin, M., Cary, S., Cowan D. 2014. High diversity of tailed phages, eukaryotic viruses and virophage-like elements in the metaviromes of Antarctic soils. Applied and Environmental Microbiology. 80(22):6888-6897.
  41. Ramond J-B, Makhalanyane TP, Tuffin MI, Cowan DA. 2015. Normalization of environmental metagenomic DNA enhances the discovery of under-represented microbial community members. Lett. Appl. Microbiol. 60(4):359.366. DOI: 10.1111/lam.12380.
  42. Adriaenssens, E., Van Zyl, L., De Maayer, P., Rubagotti, E., Rybicki, E., Tuffin, M., Cowan, D. 2015. Metagenomic analysis of the viral community in Namib Desert hypoliths. Environmental Microbiology. 17(2):480-95.
  43. Ramond J-B., Lako J., Stafford W., Tuffin M., Cowan D. 2015. Evidence of novel plant-species specific ammonia oxidizing bacterial clades in acidic South African fynbos soils. Journal of Basic Microbiology. 55 (8):1040–1047.
  44. Maropola M, Ramond J-B, Trindade M. 2015. Impact of Metagenomic DNA Extraction Procedures on the Identifiable Endophytic Bacterial Diversity in Sorghum bicolor (L. Moench). Journal of Microbiological Methods. 112:104-117.
  45. Olonade I, van Zyl L, Trindade M. 2015. Draft genome sequence of marine isolates Thalassomonas viridans and Thalassomonas actiniarum. Genome Announcements. 3(2): e00297-15.
  46. van Zyl L., Sunda F., Taylor M., Cowan D., Trindade M. 2015. Identification and characterization of a novel Geobacillus thermoglucosidasius bacteriophage, GVE3. Archives of Virology. 160(9):2269-82.
  47. Ohlhoff C, Kirby B, van Zyl L, Mutepfa D, Casanueva A, Huddy R, Bauer R, Cowan D, Tuffin M. 2015. An unusual feruloyl esterase belonging to family VIII esterases and displaying a broad substrate range. Journal of Molecular Catalysis B: Enzymatic. 118:79-88. doi:10.1016/j.molcatb.2015.04.010.
  48. Anderson D, Ferreras Eloy, Trindade M, Cowan D. 2015. A novel bacterial Water Hypersensitivity-like protein shows in vivo protection against cold and freeze damage. FEMS Microbiology Letters. 362(15):fnv110. DOI:10.1093/femsle/fnv110.
  49. Trindade M, van Zyl L, Navarro-Fernández J, Abd Elrazak A. 2015. Function-guided and targeted metagenomics as a tool to tap into marine natural product diversity for the discovery and production of drug candidates. Frontiers Microbiology. 6:1–14. doi.org/10.3389/fmicb.2015.00890.
  50. Missengue M, Musyoka N, Madzivire G, Babajide O, Fatoba O, Tuffin M, Petrik L. 2016. Leaching and antimicrobial properties of silver nanoparticles loaded onto natural zeolite clinoptilolite by ion exchange and wet impregnation. Journal of Environmental Science and Health, Part A. 51(2):97-104.
  51. van Zyl L, Taylor M, Trindade M. 2016. Engineering resistance to phage GVE3 in Geobacillus thermoglucosidasius. Applied Microbiology and Biotechnology. 100(4): 1833-1841.
  52. Adriaenssens E, van Zyl J, Cowan D, Trindade M. 2016. Metaviromics of Namib Desert Salt Pans: A Novel Lineage of Haloarchaeal Salterproviruses and a Rich Source of ssDNA Viruses. Viruses. 8(1): 14. DOI:10.3390/v8010014.
  53. van Zyl L, Matobole R, Biteghe F, Klein T, Kirby B, Trindade M. 2016. Draft Genome Sequences of Three Bacillus Species from South African Marine Sponges. Genome Announcements. 4(2). DOI: 10.1128/genomeA.00143-16.
  54. Armstrong A, Valverde A, Ramond JB, Makhalanyane T, Janssen J, Hopkins D, Aspray J, Seely M, Trindade M, Cowan D. 2016. Temporal dynamics of hot desert microbial communities reveal structural and functional responses to water input. Scientific Reports. 6: 34434. doi:10.1038/srep34434
  55. van Zyl L, Nemavhulani S, Cass J, Cowan D, Trindade M. 2016. Three novel bacteriophages isolated from the East African Rift Valley soda lakes. Virology Journal. 13:204. DOI: 10.1186/s12985-016-0656-6.
  56. Hesse U, van Heusden P, Kirby B, Olonade I, van Zyl L, Trindade M. 2017. Virome assembly and annotation: a surprise in the Namib Desert. Frontiers Microbiology. 8:13. DOI: 10.3389/fmicb.2017.00013.
  57. Matobole R, Van Zyl L, Parker-Nance S, Davies-Coleman M, Trindade M. 2017. Antibacterial activities of bacteria isolated from the marine sponges Isodictya compressa and Higginsia bidentifera collected from Algoa Bay, South Africa. Marine Drugs. 15(2):47. doi:10.3390/md15020047.
  58. Zablocki O, van Zyl L, Kirby B, Trindade M. 2017. Diversity of dsDNA viruses in a South African hot spring assessed by metagenomics and microscopy. Viruses. 9:348.
  59. Lako J, Yengkopiong Y, Stafford W, Tuffin M, Cowan D. 2018. Cloning, expression and characterization of thermostable YdaP from Bacillus licheniformis 9A. Acta Biochimica Polonica. 64:1-12.
  60. Zablocki O, van Zyl L, Trindade M. 2018. Biogeography and taxonomic overview of terrestrial hot spring thermophilic phages. Extremophiles. In press.
  61. Van Zyl L, Abrahams Y, Stander E, Kirby-McCollough B, Jourdain R, Clavaud C, Breton L, Trindade M. 2018. Novel phages of healthy skin metaviromes from South Africa. Scientific Reports. In press.

Who Am I?

I obtained my PhD in Microbiology in 2003 from the University of Cape Town (UCT), where I studied “Carbohydrate metabolism in Bifidobacterium”. For the following 3 years, I took up a post-doc position in Doug Rawlings’s Biomining Laboratory at the University of Stellenbosch, where I studied the molecular biology of heavy metal resistance in biomining organisms. I joined IMBM in 2006 as a post-doc, and was appointed Deputy Director in 2008 and Senior Lecturer in the Department of Biotechnology.

I co-ordinate the BTN 213 Food and Environmental Microbiology; BTN 312 Industrial Biotechnology; and BTN 706 Extremophiles courses at the undergraduate and Honours levels. I additionally run a short course (Microbial Ecology and Bioremediation) in the Biotechnology Masters at the Universidade Eduardo Mondlane, Moçambique..

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