Sains Malaysiana 49(10)(2020): 2335-2344
http://dx.doi.org/10.17576/jsm-2020-4910-01
Effects of
Elevated Temperature on the Tropical Soil Bacterial Diversity
(Kesan Peningkatan Suhu terhadap Kepelbagaian Bakteria Tanah Tropika)
CHIN LAI MUN1 & CLEMENTE MICHAEL WONG VUI LING1,2*
1Biotechnology
Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia
2National Antarctic
Research Centre, University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia
Received: 25 October 2019/Accepted:
22 April 2020
ABSTRACT
Bacteria are important biological components of soil that play pivotal
roles in improving soil quality and maintaining a balanced ecosystem. However,
global climate change may have severe impacts on biodiversity and ecosystems
including species loss and extinction of plants and animals, including
microbes. Thus, it is crucial to determine how elevated temperature may alter
soil bacterial diversity and composition. In this study, an in vitro simulated temperature
rise experiment was carried out on soils from three sampling sites, referring
to S1, S2, and S3 around Sabah, Malaysia. Soils were incubated at 25 °C (control)
and 27 °C (simulated warming) with constant parameters in a growth chamber up
to 16 months. Total DNA was extracted from microbes in the soil and used for
PCR amplification targeting the V3-V4 region of the 16S rRNA gene. These
amplicons were sequenced using the MiSeq platform
(Illumina, USA). Raw DNA sequences were trimmed, merged, and aligned against
the 16S rRNA sequences in the NCBI 16S database. The results showed that the
analyzed soils were mainly dominated by Proteobacteria, Actinobacteria, Acidobacteria, and Verrucomicrobia. After
16 months of simulated warming, a net decrease of Proteobacteria, Acidobacteria, and Planctomycetes, and
an increase of Actinobacteria and Chloroflexi were observed for all three soil samples,
indicating that these phyla were highly affected by a temperature rise. At the
genus level, Gaiella and Nocardioides exhibited a net increase while Bradyrhizobium,
Mycobacterium, Tepidisphaera, and Paludibaculum demonstrated net decrease after 16 months of simulated warming.
Knowledge on the changes of soil bacterial diversity patterns as a result of
temperature elevation will contribute to select the best intervention strategy
to overcome global warming issue in the future.
Keywords: 16S
metagenomic sequencing; growth chamber; soil bacteria; temperature
ABSTRAK
Bakteria merupakan komponen biologi penting yang memainkan peranan dalam meningkatkan kualiti tanah dan mengekalkan keseimbangan ekosistem. Akan tetapi, perubahan iklim global mungkin akan memberi kesan buruk terhadapkepelbagaian bio dan ekosistem termasuk kehilangan spesies serta kepupusan haiwan, tumbuhan dan mikrob. Oleh itu, adalah penting untuk menentukan bagaimana peningkatan suhu akan menyebabkan perubahan kepelbagaian dan komposisi bakteria dalam tanah. Dalam kajian ini, uji kajisimulasi peningkatan suhu secarain vitro telah dijalankan ke atas tanah yang diperoleh dari tiga tapak pensampelan di sekitar Sabah, Malaysia. Tanah tersebut dieram pada suhu 25 °C (kawalan) dan 27 °C (simulasi) dengan parameter yang sama dalam kebuk pertumbuhan selama 16 bulan. DNA keseluruhan telah diekstrak daripada mikrob dalam tanah dan digunakan untuk amplifikasi PCR menyasarkan kawasan V3-V4 pada gen
16 SrRNA. Amplikon tersebut dijujuk dengan menggunakan platform Miseq (Illumina, USA). Data penjujukan telah dipangkas, digabungkan dan disejajarkan dengan jujukan 16 SrRNA pada pangkalan data 16S NCBI. Hasil kajian menunjukkan bahawa sampel tanah didominasi oleh Proteobacteria, Actinobacteria, Acidobacteria dan Verrucomicrobia. Selepas simulasi pemanasan selama 16 bulan, pengurangan bersih bagi Proteobacteria, Acidobacteria dan Planctomycetes serta peningkatan bagi Actinobacteria dan Chloroflexi dapat diperhatikan untuk ketiga-tiga sampel tanah. Pada peringkat genus, Gaiella dan Nocardioides menunjukkan peningkatan bersih manakala Bradyrhizobium,
Mycobacterium, Tepidisphaera dan Paludibaculum menunjukkan penurunan bersih selepas 16 bulan. Pengetahuan corak perubahankepelbagaian bakteria dalam tanah akibat peningkatan suhu persekitaran akan dapat membantu dalam strategi intervensi ke atas tanah bagi menangani isu pemanasan global pada masa hadapan.
Kata kunci: Bakteria tanah; kebuk pertumbuhan; penjujukan metagenomik 16S; suhu
REFERENCES
Aislable,
J. & Deslippe, J.R. 2013. Soil microbes and their
contribution to soil services. In Ecosystem Services in New Zealand-Conditions and Trends, edited by Dymond, J. Lincoln, New Zealand: Manaaki Whenua Press.
Albuquerque,
L., França, L., Rainey, F.A., Schumann, P., Nobre, M.F. & da Costa, M.S. 2011. Gaiella occulta gen. nov., sp. nov., a novel representative of a deep branching
phylogenetic lineage within the class Actinobacteria and proposal of Gaiellaceae fam. nov. and Gaiellales ord. nov. Systematic
and Applied Microbiology 34(8): 595-599.
Baker-Austin, C.,
Stockley, L., Rangdale, R. & Martinez-Urtaza, J. 2010. Environmental occurrence and clinical
impact of Vibrio vulnificus and Vibrio parahaemolyticus: A European perspective. Environmental Microbiology Reports 2(1): 7-18.
Carlin,
F., Brillard, J., Broussolle,
V., Clavel, T., Duport, C.,
Jobin, M., Guinebretière, M., Auger, S., Sorokine, A. & Nugyen-Thé, C.
2010. Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a
changing environment. Food Research International 43(7): 1885-1894.
Classen, A.T., Sundqvist,
M.K., Henning, J.A., Newman, G.S., Moore, J.A., Cregger, M.A.,
Moorhead, L.C. & Patterson, C.M. 2015. Direct and indirect effects of
climate change on soil microbial and soil microbial‐plant interactions:
What lies ahead? Ecosphere 6(8): 1-21.
Colwell, R.R. 1996. Global
climate and infectious disease: The cholera paradigm. Science 274(5295):
2025-2031.
Hayat,
R., Ali, S., Amara, U., Khalid, R. & Ahmed, I. 2010. Soil beneficial
bacteria and their role in plant growth promotion: A review. Annals
Microbiology 60(4): 579-598.
Heuer, H., Krsek, M., Baker, P., Smalla, K. & Wellington, E.M. 1997. Analysis of
actinomycete communities by specific amplification of genes encoding 16S rRNA
and gel-electrophoretic separation in denaturing gradients. Applied and
Environmental Microbiology 63(8): 3233-3241.
Huson,
D.H., Mitra, S., Weber, N., Ruscheweyh,
H.J. & Schuster, S.C. 2011. Integrative analysis of environmental sequences
using MEGAN 4. Genome Research 21(9): 1552-1560.
IPCC. 2018. Global
Warming of 1.5°C. In An IPCC Special Report on the Impacts of Global Warming of 1.5°C above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty, edited by Masson-Delmotte, V., Zhai, P., Pörtner, H.O., Roberts,
D., Skea, J., Shukla, P.R., Pirani, A., Moufouma-Okia, W., Péan, C., Pidcock, R., Connors, S., Matthews, J.B.R., Chen, Y., Zhou,
X., Gomis, M.I., Lonnoy,
E., Maycock, T., Tignor, M.
& Waterfield, T. https://www.ipcc.ch/site/assets/uploads/sites/2/2019/06/SR15_Full_Report_High_Res.pdf.
Jeanbille, M., Buée, M., Bach, C., Cébron, A.,
Frey-Klett, P., Turpault,
M.P. & Uroz, S. 2016. Soil parameters drive the
structure, diversity and metabolic potentials of the bacterial communities
across temperate beech forest soil sequences. Microbial Ecology 71(2):
482-493.
Jenkins, S.N., Waite, I.S., Blackburn, A., Husband, R.,
Rushton, S.P., Manning, D.C. & O’Donnell, A.G. 2009. Actinobacterial
community dynamics in long term managed grasslands. Antonie Van Leeuwenhoek 95(4): 319-334.
Kerfahi,
D., Tripathi, B.M., Dong, K., Go, R. & Adams, J.M. 2016. Rainforest
conversion to rubber plantation may not result in lower soil diversity of
bacteria, fungi, and nematodes. Microbial Ecology 72(2): 359-371.
Kim,
M., Kim, W.S., Tripathi, B.M. & Adams, J. 2014. Distinct bacterial
communities dominate tropical and temperate zone leaf litter. Microbial
Ecology 67(4): 837-848.
Klindworth, A., Pruesse,
E., Schweer, T., Peplies,
J., Quast, C., Horn, M. & Glöckner, F.O. 2013.
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next
generation sequencing-based diversity studies. Nucleic Acids Research 41(1): 1-11.
Lugtenberg, B. & Kamilova, F. 2009.
Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63:
541-556.
Mateos-Rivera,
A., Yde, J.C., Wilson, B., Finster,
K.W., Reigstad, L.J. & Øvreås,
L. 2016. The effect of temperature change on the microbial diversity and
community structure along the chronosequence of the
sub-arctic glacier forefield of Styggedalsbreen (Norway). FEMS Microbiology Ecology 92(4): 1-13.
NOAA.
2020. National Centers for Environmental Information, State of the Climate:
Global Climate Report for Annual 2019. https://www.ncdc.noaa.gov/sotc/global/201913. Accessed on 18 February 2020.
NOAA/ESRL.
2010. Use of NOAA/ESRL data. Earth System Research Laboratory, National Oceanic
and Atmospheric Administration, United States. Department of Commerce, Boulder,
Colorado. United States of America.
Novello, G., Gamalero, E., Bona, E., Boatti,
L., Mignone, F., Massa, N., Cesaro,
P., Lingua, G. & Berta, G. 2017. The rhizosphere bacterial microbiota of Vitis
vinifera cv. pinot noir in an integrated pest management vineyard. Frontiers
in Microbiology 8: 1528.
Pearce, D.A., Hodgson, D.A., Thorne, M.A., Burns, G. & Cockell, C.S. 2013. Preliminary analysis of life within a
former subglacial lake sediment in Antarctica. Diversity 5(3):
680-702.
Rinnan, R., Michelsen, A., Bååth, E. & Jonasson, S.
2007. Fifteen years of climate change manipulations alter soil microbial
communities in a subarctic heath ecosystem. Global Change Biology 13(1):
28-39.
Ryu, C.M., Farag, M.A., Hu, C.H.,
Reddy, M.S., Wei, H.X., Paré, P.W. & Kloepper, J.W. 2003. Bacterial
volatiles promote growth in Arabidopsis. Proceedings of the
National Academy of Sciences of the United States of America 100(8):
4927-4932.
Schloss, P.D. & Handelsman, J.
2005. Metagenomics for studying unculturable microorganisms: Cutting the
Gordian knot. Genome
Biology 6(8): 229.
Schuette, U.M., Abdo, Z., Foster, J., Ravel, J., Bunge, J.,
Solheim, B. & Forney, L.J. 2010. Bacterial diversity in a glacier foreland
of the high Arctic. Molecular Ecology 19: 54-66.
Schuur, E.A.G., Bockheim,
J., Canadell, J.G., Euskirchen,
E., Field, C.B., Goryachkin, S.V., Hagemann, S., Kuhry, P., Lafleur,
P.M., Lee, H., Mazhitova, G., Nelson, F.E., Rinke,
A., Romanovsky, V.E., Shiklomanov,
N., Tarnocai, C., Venevsky,
S., Vogel, J.G. & Zimov, S.A. 2008. Vulnerability
of permafrost carbon to climate change: Implications for the
global carbon cycle. Bioscience 58(8): 701-714.
Shao, J., Li, S., Zhang, N., Cui, X., Zhou, X., Zhang,
G., Shen, Q. & Zhang, R. 2015. Analysis and cloning of the synthetic
pathway of the phytohormone indole-3-acetic acid in the plant-beneficial Bacillus amyloliquefaciens SQR9. Microbial Cell
Factories 14(1): 130.
Sheik, C.S., Beasley, W.H., Elshahed,
M.S., Zhou, X., Luo, Y. & Krumholz, L.R. 2011.
Effect of warming and drought on grassland microbial communities. International Society
for Microbial Ecology ISEME 5(10):
1692.
Skidmore, M., Anderson, S.P., Sharp, M., Foght,
J. & Lanoil, B.D. 2005. Comparison of microbial
community compositions of two subglacial environments reveals a possible role
for microbes in chemical weathering processes. Applied and
Environmental Microbiology 71(11): 6986-6997.
Smeds,
L. & Künstner, A. 2011. ConDeTri - A content dependent read trimmer for illumina data. PLoS ONE 6(10): e26314.
Thwaite, J.E. & Atkins, H.S. 2012. Bacillus: Anthrax; food
poisoning. In Medical Microbiology
(18th edition) - A Guide to Microbial Infection: Pathogenesis, Immunity, Laboratory Investigation and Control, edited by Greenwood, D., Slack, R., Michaelm, B. & Irving, W. London: Churchill Livingstone Elsevier. pp. 237-244.
Torsvik, V., Øvreås, L. & Thingstad, T.F.
2002. Prokaryotic diversity--magnitude, dynamics, and controlling
factors. Science 296(5570): 1064-1066.
Trivedi, P., Delgado-Baquerizo, M., Anderson, I.C. & Singh, B.K. 2016.
Response of soil properties and microbial communities to agriculture: Implications for primary productivity and soil health indicators. Frontiers
in Plant Science 7: 990.
Verma, J.P., Yadav, J.,
Tiwari, K.N. & Lavakush, S.V. 2010. Impact of
plant growth promoting rhizobacteria on crop production. International
Journal of Agricultural Research 5(11): 954-983.
Wang, N.F., Zhang, T., Zhang, F., Wang, E.T., He,
J.F., Ding, H., Zhang, B.T., Liu, J., Ran, X.B. & Zang, J.Y. 2015.
Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454
pyrosequencing. Frontiers in Microbiology 6: 1188.
Ward, N.L., Challacombe, J.F.,
Janssen, P.H., Henrissat, B., Coutinho, P.M., Wu, M., Xie, G., Haft, D.H., Sait,
M., Badger, J.
& Barabote, R.D. 2009. Three
genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied and Environmental Microbiology 75(7): 2046-2056.
Yergeau, E., Bokhorst, S.,
Kang, S., Zhou, J., Greer, C.W., Aerts, R. & Kowalchuk, G.A. 2012. Shifts in soil microorganisms in
response to warming are consistent across a range of Antarctic environments. International Society
for Microbial Ecology ISEME 6(3): 692-702.
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. 2014. PEAR: A fast and accurate Illumina paired-end read merger. Bioinformatics 30(5):
614-620.
Zhang, W., Parker,
K.M., Luo, Y., Wan, S., Wallace, L.L. & Hu, S. 2005. Soil microbial
responses to experimental warming and clipping in a tallgrass prairie. Global Change Biology 11(2): 266-277.
Zhang, X., Zhang, G., Chen, Q. & Han, X. 2013. Soil
bacterial communities respond to climate changes in a temperate steppe. PLoS ONE 8(11): e78616.
Zumsteg, A., Bååth, E., Stierli, B., Zeyer, J. & Frey, B. 2013. Bacterial and fungal
community responses to reciprocal soil transfer along a temperature and soil
moisture gradient in a glacier forefield. Soil
Biology Biochemistry 61: 121-132.
*Corresponding
author; email: michaelw@ums.edu.my