Abstract—
The cacao plantations in Sulawesi Island, Indonesia are responsible for a great part of the local economy; however, their soils still need to be deeply explored. Our study focused on evaluation of the microbial communities in cacao soils according to their location and applied management system. Four soil samples were taken from six cacao farms under two kinds of systems (conventional and organic). 16S and ITS rDNA amplicon sequencing analyses of soils were also performed to identify bacteria and fungi, respectively, whereby their relative abundance and diversity were determined. In general view, the bacterial and fungal communities were affected by management system at the local and general levels. Bacterial analyses indicated that the number of operational taxonomic units and bacterial diversity were higher under the organic system in Kulawi, Palolo, and Poso farms. The composition and biodiversity of fungi were clearly different between organic and conventional systems and between different places (coastal and inland). The effect of agricultural management was observed in each location individually and in general.
Similar content being viewed by others
REFERENCES
A. F. Cruz, I. N. Suwastika, H. Sasaki, T. Uchiyama, N. A. Pakawaru, W. Wijayanti, Z. Basri, Y. Ishizaki, and T. Shiina, “Cacao plantations on Sulawesi Island, Indonesia: I—an agro-ecological analysis of conventional and organic farms,” Org. Agric. 9 (2), 225–234 (2019).
A. H. C. van Bruggen, M. He, V. V. Zelenev, V. M. Semenov, A. M., Semenov, E. V. Semenova, T. V. Kuznetsova, A. K. Khozaeva, A. M. Kuznetsov, and M. V. Semenov, “Relationships between greenhouse gas emissions and cultivable bacterial populations in conventional, organic and long-term grass plots as affected by environmental variables and disturbances,” Soil Biol. Biochem. 114, 145–159 (2017).
A. M. Semenov, I. A. Bubnov, V. M. Semenov, E. V. Semenova, V. V. Zelenev, and N. A. Semenova, “Daily dynamics of bacterial numbers, CO2 emissions from soil and relationships between their wavelike fluctuations and succession of the microbial community,” Eurasian Soil Sci. 46, 869–884 (2013).
A. Orgiazzi, V. Bianciotto, P. Bonfante, S. Daghino, S. Ghignone, A. Lazzari, E. Lumini, A. Mello, C. Napoli, S. Perotto, A. Vizzini, S. Bagella, C. Murat, and M. Girlanda, “454 pyrosequencing analysis of fungal assemblages from geographically distant, disparate soils reveals spatial patterning and a core mycobiome,” Diversity 5, 73–98 (2013).
C. Luo, D. Tsementzi, N. Kyrpides, T. Read, K. T. Konstantinidis, C. Luo, D. Tsementzi, N. Kyrpides, T. Read, and K. Konstantinidis, “Direct comparisons of Illumina vs. Roche 454 sequencing technologies on the same microbial community DNA sample,” PLoS One 7, e30087 (2012).
C. Will, A. Thurmer, A. Wollherr, H. Nacke, N. Herold, M. Schrumpf, J. Gutknecht, T. Wubet, F. Buscot, and R. Daniel, “Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes,” Appl. Environ. Microbiol. 76, 6751–6759 (2010).
D. N. Chavarria, C. Pérez-Brandan, D. L. Serri, J. M. Meriles, S. B. Restovich, A. E. Andriulo, L. Jacquelin, and S. Vargas-Gil, “Response of soil microbial communities to agroecological versus conventional systems of extensive agriculture,” Agric. Ecosyst. Environ. 264, 1–8 (2018).
D. Thakuria, O. Schmidt, M. Mac Siúrtáin, D. Egan, and F. M. Doohan, “Importance of (DNA) quality in comparative soil microbial community structure analyses,” Soil Biol. Biochem. 40, 1390–1403 (2008).
FAO, Food Agriculture Organization, GeoNetwork. http://www.fao.org/geonetwork/srv/en/main.home.
G. Rastogi, J. J. Tech, G. L. Coaker, and J. H. J. Leveau, “A PCR-based toolbox for the culture-independent quantification of total bacterial abundances in plant environments,” J. Microbiol. Methods 83, 127–132 (2010).
H. Wasserstrom, S. Kublik, R. Wasserstrom, S. Schulz, M. Schloter, and Y. Steinberger, “Bacterial community composition in costal dunes of the Mediterranean along a gradient from the sea shore to the inland,” Sci. Rep. 7, 40266 (2017).
I. Douterelo, J. B. Boxall, P. Deines, R. Sekar, K. E. Fish, and C. A. Biggs, “Methodological approaches for studying the microbial ecology of drinking water distribution systems,” Water Res. 65, 134–156 (2014).
I. Nabhani, A. Daryanto, M. Yassin, and A. Rifin, “Can Indonesia cocoa farmers get benefit on global value chain inclusion?” Asian Soc. Sci. 11, 288–294 (2015).
J. Cong, Y. Yang, X. Liu, H. Lu, X. Liu, J. Zhou, D. Li, H. Yin, J. Ding, and Y. Zhang, “Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession,” Sci. Rep. 5, 10007 (2015).
J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Pena, J. K. Goodrich, and J. I. Gordon, “QIIME allows analysis of high-throughput community sequencing data,” Nat Methods 7 (5), 335–336 (2010).
J. Sylla, B. W. Alsanius, E. Kruger, A. Reineke, S. Strohmeier, and W. Wohanka, “Leaf microbiota of strawberries as affected by biological control agents,” Phytopathology 103, 1001–1011 (2013).
K. Xue, L. Wu, Y. Deng, Z. He, J. van Nostrand, P. G. Robertson, T. M. Schmidt, and J. Zhou, “Functional gene differences in soil microbial communities from conventional, low-input, and organic farmlands,” Appl. Environ. Microbiol. 79, 1284–1292 (2013).
L. B. Martínez-García, G. Korthals, L. Brussaard, H. B. Jørgensen, and G. B. De Deyn, “Organic management and cover crop species steer soil microbial community structure and functionality along with soil organic matter properties,” Agric. Ecosyst. Environ. 263, 7–17 (2018).
L. M. H. Kilowasid, T. S. Syamsudin, E. Sulystiawati, and F. X. Susilo, “Structure of soil food web in smallholder cocoa plantation, South Konawe district, Southeast Sulawesi, Indonesia,” Agrivita, J. Agric. Sci. 36, 33–47 (2014).
M. Buée, M. Reich, C. Murat, E. Morin, R. H. Nilsson, S. Uroz, and F. Martin, “Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity,” New Phytol. 184, 449–456 (2009).
M. Hartmann, B. Frey, J. Mayer, P. Mader, and F. Widmer, “Distinct soil microbial diversity under long-term organic and conventional farming,” ISME J. 9, 1177–1194 (2015).
M. He, W. Ma, V. V. Zelenev, A. K. Khodzaeva, A. M. Kuznetsov, A. M. Semenov, V. M. Semenov, W. Blok, and A. H. C. van Bruggen, “Short-term dynamics of greenhouse gas emissions and cultivable bacterial populations in response to induced and natural disturbances in organically and conventionally managed soils,” Appl. Soil Ecol. 119, 294–306 (2017).
M. Oudah, and A. Henschel, “Taxonomy-aware feature engineering for microbiome classification,” BMC Bioinf. 19, 227 (2018).
M. V. Semenov, T. I. Chernov, A. K. Tkhakakhova, A. D. Zhelezova, E. A. Ivanova, T. V. Kolganova, and O. V. Kutovaya, “Distribution of prokaryotic communities throughout the Chernozem profiles under different land uses for over a century,” Appl. Soil Ecol. 127, 8–18 (2018).
M. S. Strickland and J. Rousk, “Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications,” Soil Biol. Biochem. 42, 1385–1395 (2010).
R. Daniel, “The metagenomics of soil,” Nat. Rev. Mic-ro. 3, 470–478 (2005).
S. Dequiedt, N. P. A. Saby, M. Lelievre, C. Jolivet, J. Thioulouse, B. Toutain, D. Arrouays, A. Bispo, P. Lemanceau, and L. Ranjard, “Biogeographical patterns of soil molecular microbial biomass as influenced by soil characteristics and management,” Global Ecol. Biogeogr. 20, 641 (2011).
S. J. Kemmitt, D. Wright, K. W. T. Goulding, and D. L. Jones, “pH regulation of carbon and nitrogen dynamics in two agricultural soils,” Soil Biol. Biochem. 38, 898–911 (2006).
S. V Angiuoli, M. Matalka, A. Gussman, K. Galens, M. Vangala, D. R. Riley, C. Arze, J. R. White, O. White, and W. F. Fricke, “CloVR: a virtual machine for automated and portable sequence analysis from the desktop using cloud computing,” BMC Bioinf. 12, 356 (2011).
S. Yoshitake and T. Nakatsubo, “Changes in soil microbial biomass and community composition along vegetation zonation in a coastal sand dune,” Soil Res. 46, 390–396 (2008).
T. I. Chernov, A. K. Tkhakakhova, E. A. Ivanova, O. V. Kutovaya, and V. I. Turusov, “Seasonal dynamics of the microbiome of chernozems of the long-term agrochemical experiment in Kamennaya Steppe,” Eurasian Soil Sci. 48, 1349–1353 (2015).
V. O. Biederbeck, C. A. Campbell, V. Rasiah, R. P. Zentner, and G. Wen, “Soil quality attributes as influenced by annual legumes used as green manure,” Soil Biol. Biochem. 30, 1177–1185 (1998).
V. O. Biederbeck, R. P. Zentner, and C. A. Campbell, “Soil microbial populations and activities as influenced by legume green fallow in a semiarid climate,” Soil Biol. Biochem. 37, 1775–1784 (2005).
W. Wang, H. Wang, Y. Feng, L. Wang, X. Xiao, Y. Xi, X. Luo, R. Sun, X. Ye, Y. Huang, Z. Zhang, and Z. Cui, “Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River,” Sci. Rep. 6, 35046 (2016).
X. Luo, X. Fu, Y. Yang, P. Cai, S. Peng, W. Chen, and Q. Huang, “Microbial communities play important roles in modulating paddy soil fertility,” Sci. Rep. 6, 20326 (2016).
ACKNOWLEDGMENTS
We would like to thank the cacao farmers in Sulawesi, Indonesia, for allowing us to sample in their areas. We would also like to thank the students at Tadulako University who assisted us with sampling and analysis. Finally, we are thankful to Dr. Geleta Dugassa Markaof Universidade Federal de Vicosa, Brasil, for the constructive comments of this manuscript. This project was supported by the bilateral cooperation program between JSPS (Japan) and DHGE (Indonesia), and another grant of International collaboration.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary materials are available for this at doi: 10.1134/S1064229319100144 and are accessible for authorized users.
Supplementary material
Rights and permissions
About this article
Cite this article
Suwastika, I.N., Cruz, A.F., Pakawaru, N.A. et al. Characterization of Bacterial and Fungal Communities in Soils under Different Farming Systems. The Cacao Plantation in Sulawesi Island—Indonesia. Eurasian Soil Sc. 52, 1234–1243 (2019). https://doi.org/10.1134/S1064229319100144
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1064229319100144