Characterization of Bacterial and Fungal Communities in Soils under Different Farming Systems. The Cacao Plantation in Sulawesi Island—Indonesia


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.

This is a preview of subscription content, log in to check access.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.


  1. 1

    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).

    Article  Google Scholar 

  2. 2

    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).

    Article  Google Scholar 

  3. 3

    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).

    Article  Google Scholar 

  4. 4

    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).

    Article  Google Scholar 

  5. 5

    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).

    Article  Google Scholar 

  6. 6

    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).

    Article  Google Scholar 

  7. 7

    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).

    Article  Google Scholar 

  8. 8

    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).

    Article  Google Scholar 

  9. 9

    FAO, Food Agriculture Organization, GeoNetwork.

  10. 10

    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).

    Article  Google Scholar 

  11. 11

    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).

    Article  Google Scholar 

  12. 12

    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).

    Article  Google Scholar 

  13. 13

    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).

    Article  Google Scholar 

  14. 14

    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).

    Article  Google Scholar 

  15. 15

    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).

    Article  Google Scholar 

  16. 16

    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).

    Article  Google Scholar 

  17. 17

    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).

    Article  Google Scholar 

  18. 18

    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).

    Article  Google Scholar 

  19. 19

    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).

    Google Scholar 

  20. 20

    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).

    Article  Google Scholar 

  21. 21

    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).

    Article  Google Scholar 

  22. 22

    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).

    Article  Google Scholar 

  23. 23

    M. Oudah, and A. Henschel, “Taxonomy-aware feature engineering for microbiome classification,” BMC Bioinf. 19, 227 (2018).

    Article  Google Scholar 

  24. 24

    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).

    Article  Google Scholar 

  25. 25

    M. S. Strickland and J. Rousk, “Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications,” Soil Biol. Biochem. 42, 1385–1395 (2010).

    Article  Google Scholar 

  26. 26

    R. Daniel, “The metagenomics of soil,” Nat. Rev. Mic-ro. 3, 470–478 (2005).

    Article  Google Scholar 

  27. 27

    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).

    Article  Google Scholar 

  28. 28

    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).

    Article  Google Scholar 

  29. 29

    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).

    Article  Google Scholar 

  30. 30

    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).

    Article  Google Scholar 

  31. 31

    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).

    Article  Google Scholar 

  32. 32

    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).

    Article  Google Scholar 

  33. 33

    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).

    Article  Google Scholar 

  34. 34

    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).

    Article  Google Scholar 

  35. 35

    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).

    Article  Google Scholar 

Download references


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



Corresponding author

Correspondence to A. F. Cruz.

Additional information

Supplementary materials are available for this at doi: 10.1134/S1064229319100144 and are accessible for authorized users.

Supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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).

Download citation


  • agricultural management
  • amplicon sequencing
  • location
  • microbial diversity