Abstract
Purpose
Understanding soil heterotrophic respiration in relation to microbial properties is not only fundamental to soil respiration modelling, prediction, and regulation through management, but also essential to interpreting microbial community dynamics from an ecologically meaningful perspective. This paper reviewed the recent advances in knowledge and proposed future directions for exploring the respiration-microbe relationships by means of rDNA- or rRNA-based indices (i.e. rDNA copies, rRNA copies, and rDNA- or rRNA-based community structures).
Materials and methods
We first elucidated the theoretical basis for using rDNA- or rRNA-based indices to probe into soil microbial respiration. Then, the published studies that simultaneously measured soil microbial respiration and the rDNA- or rRNA-based indices were synthesized, extracted, and analysed to further explore the respiration-microbe relationships. At last, the uncertainties and perspectives for establishing the respiration-microbe links were proposed and discussed.
Results and discussion
The rDNA- or rRNA-based indices are theoretically promising for pinpointing the relationships between soil heterotrophic respiration and microbial properties. Our systematic review suggested that the correlations between bacterial rDNA copies and microbial respiration are inconsistent across studies, while the fungal and archaeal rDNA (or ITS) copies showed moderately positive and negative correlations with soil microbial respiration, respectively. Bacterial 16S rDNA-based community structures were significantly correlated with soil microbial respiration in some studies, but not in some short-term situations. Although rRNA copies are widely used as the proxies of microbial activity, no significant correlations between rRNA copies and soil microbial respiration have been found in previous studies. Bacterial 16S rRNA-based community structures were correlated well with the short-term responses of soil microbial respiration to rewetting or labile carbon amendments and clearly outperformed other rDNA- or rRNA-based indices. As respiration-microbe relationships can be affected by many factors, such as soil physicochemical properties and even the analysis methods of microbial indices, the 69 previous studies included in this review actually provided limited information on them, and the aforementioned results still need to be further confirmed in future studies.
Conclusions and perspectives
Overall, the relationships between soil microbial respiration and rDNA- or rRNA-based indices are still far from being well established. Future research should be directed to systematically understanding the respiration-microbe links, with more attention to the fungus-, archaea- and RNA-related molecular indices. The relationships between microbial specific lineages and total respiration rates should be explored in future studies, and the effects of edaphic properties on the respiration-microbe relationships should also be evaluated.
This is a preview of subscription content, access via your institution.



References
Amend AS, Martiny AC, Allison SD, Berlemont R, Goulden ML, Lu Y (2016) Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. ISME J 10:109–118
Anderson IC, Parkin PI (2007) Detection of active soil fungi by RT-PCR amplification of precursor rRNA molecules. J Microbiol Methods 68:248–253
Andert J, Mumme J (2015) Impact of pyrolysis and hydrothermal biochar on gas-emitting activity of soil microorganisms and bacterial and archaeal community composition. Appl Soil Ecol 96:225–239
Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, Vetrovsky T, Zifcakova L, Snajdr J, Ridl J, Vlcek C, Voriskova J (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6:248–258
Bernard L, Mougel C, Maron PA, Nowak V, Leveque J, Henault C, Haichar FEZ, Berge O, Marol C, Balesdent J, Gibiat F, Lemanceau P, Ranjard L (2007) Dynamics and identification of soil microbial populations actively assimilating carbon from 13C-labelled wheat residue as estimated by DNA- and RNA-SIP techniques. Environ Microbiol 9:752–764
Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241
Barnard RL, Osborne CA, Firestone MK (2015) Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate. ISME J 9:946–957
Bier RL, Bernhardt ES, Boot CM, Graham EB, Hall EK, Lennon JT, Nemergut DR, Osborne BB, Ruiz-González C, Schimel JP (2015) Linking microbial community structure and microbial processes: an empirical and conceptual overview. FEMS Microbiol Ecol 91:fiv113
Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211
Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7:2061–2068
Blazewicz SJ, Schwartz E, Firestone MK (2014) Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95:1162–1172
Bond-Lamberty B, Wang CK, Gower ST (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Glob Chang Biol 10:1756–1766
Bru D, Martin-Laurent F, Philippot L (2008) Quantification of the detrimental effect of a single primer-template mismatch by real-time PCR using the 16S rRNA gene as an example. Appl Environ Microbiol 74:1660–1663
Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti M (2005) Impact of Bt corn on rhizospheric and on beneficial mycorrhizal symbiosis and soil eubacterial communities iosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729
Castro HF, Classen AT, Austin EE, Crawford KM, Schadt CW (2012) Development and validation of a citrate synthase directed quantitative PCR marker for soil bacterial communities. Appl Soil Ecol 61:69–75
Cesarz S, Fender AC, Beyer F, Valtanen K, Pfeiffer B, Gansert D, Hertel D, Polle A, Daniel R, Leuschner C, Scheu S (2013) Roots from beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) differentially affect soil microorganisms and carbon dynamics. Soil Biol Biochem 61:23–32
Che RX, Deng YC, Wang F, Wang WJ, ZH X, Wang YF, Cui XY (2015) 16S rRNA-based bacterial community structure is a sensitive indicator of soil respiration activity. J Soils Sediments 15:1987–1990
Che RX, Wang F, Wang YF, Deng YC, Zhang J, Ma S, Cui XY (2016) A review on the methods for measuring total microbial activity in soils. Acta Entomol Sin 36:2103–2112
Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240
Cleveland CC, Reed SC, Keller AB, Nemergut DR, O’Neill SP, Ostertag R, Vitousek PM (2014) Litter quality versus soil microbial community controls over decomposition: a quantitative analysis. Oecologia 174:283–294
de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064
Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, Hugenholtz P (2010) Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4:642–647
Evans SE, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116
Evans SE, Wallenstein MD, Burke IC (2014) Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought? Ecology 95:110–122
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
Goberna M, Garcia C, Insam H, Hernandez M, Verdu M (2012) Burning fire-prone mediterranean shrublands: immediate changes in soil microbial community structure and ecosystem functions. Microb Ecol 64:242–255
Graham EB, Wieder WR, Leff JW, Weintraub SR, Townsend AR, Cleveland CC, Philippot L, Nemergut DR (2014) Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes. Soil Biol Biochem 68:279–282
Graharni EB et al (2016) Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol. doi:10.3389/fmicb.2016.00214
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
Imparato V, Santos SS, Johansen A, Geisen S, Winding A (2016) Stimulation of bacteria and protists in rhizosphere of glyphosate-treated barley. Appl Soil Ecol 98:47–55
IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge and New York
Kaplan H, Ratering S, Hanauer T, Felix-Henningsen P, Schnell S (2014) Impact of trace metal contamination and in situ remediation on microbial diversity and respiratory activity of heavily polluted Kastanozems. Biol Fertil Soils 50:735–744
Kerkhof L, Kemp P (1999) Small ribosomal RNA content in marine Proteobacteria during non-steady-state growth. FEMS Microbiol Ecol 30:253–260
Kim TG, Jeong S-Y, Cho K-S (2014) Comparison of droplet digital PCR and quantitative real-time PCR for examining population dynamics of bacteria in soil. Appl Microbiol Biotechnol 98:6105–6113
Lahtinen SJ, Ahokoski H, Reinikainen JP, Gueimonde M, Nurmi J, Ouwehand AC, Salminen SJ (2008) Degradation of 16S rRNA and attributes of viability of viable but nonculturable probiotic bacteria. Lett Appl Microbiol 46:693–698
Leff JW, Nemergut DR, Grandy AS, O’Neill SP, Wickings K, Townsend AR, Cleveland CC (2012) The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems 15:284–298
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130
Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Dunfield KE (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39:2977–2991
Lewin B (2004) Genes VIII. Prentice Hall, Saddle River
Li XF, You F, Bond PL, Huang LB (2015) Establishing microbial diversity and functions in weathered and neutral Cu-Pb-Zn tailings with native soil addition. Geoderma 247:108–116
Lima ACR, Brussaard L, Totola MR, Hoogmoed WB, de Goede RGM (2013) A functional evaluation of three indicator sets for assessing soil quality. Appl Soil Ecol 64:194–200
Lindemann SR, Bernstein HC, Song H-S, Fredrickson JK, Fields MW, Shou W, Johnson DR, Beliaev AS (2016) Engineering microbial consortia for controllable outputs. ISME J. doi:10.1038/ismej.2016.26
Liu YZ, Zhou T, Crowley D, Li LQ, Liu DW, Zheng JW, Yu XY, Pan GX, Hussain Q, Zhang XH, Zheng JF (2012) Decline in topsoil microbial quotient, fungal abundance and C utilization efficiency of rice paddies under heavy metal pollution across south China. PLoS One. doi:10.1371/journal.pone.0038858
Maila MP, Randima P, Surridge K, Dronen K, Cloete TE (2005) Evaluation of microbial diversity of different soil layers at a contaminated diesel site. Int Biodeterior Biodegr 55:39–44
Martin JF, Barreiro C, Gonzalez-Lavado E, Barriuso M (2003) Ribosomal RNA and ribosomal proteins in corynebacteria. J Biotechnol 104:41–53
Martiny AC, Treseder K, Pusch G (2013) Phylogenetic conservatism of functional traits in microorganisms. ISME J 7:830–838
Morrissey EM, McHugh TA, Preteska L, Hayer M, Dijkstra P, Hungate BA, Schwartz E (2015) Dynamics of extracellular DNA decomposition and bacterial community composition in soil. Soil Biol Biochem 86:42–49
Morrissey EM, Mau RL, Schwartz E, Caporaso JG, Dijkstra P, van Gestel N, Koch BJ, Liu CM, Hayer M, McHugh TA (2016) Phylogenetic organization of bacterial activity. ISME J. doi:10.1038/ismej.2016.28
Muttray AF, Mohn WW (1999) Quantitation of the population size and metabolic activity of a resin acid degrading bacterium in activated sludge using slot-blot hybridization to measure the rRNA:rDNA ratio. Microb Ecol 38:348–357
Nazaries L, Tottey W, Robinson L, Khachane A, Abu Al-Soud W, Sorensen S, Singh BK (2015) Shifts in the microbial community structure explain the response of soil respiration to land-use change but not to climate warming. Soil Biol Biochem 89:123–134
Nogueira MA, Albino UB, Brandao-Junior O, Braun G, Cruz MF, Dias BA, Duarte RTD, Gioppo NMR, Menna P, Orlandi JM, Raimam MP, Rampazo LGL, Santos MA, Silva MEZ, Vieira FP, Torezan JMD, Hungria M, Andrade G (2006) Promising indicators for assessment of agroecosystems alteration among natural, reforested and agricultural land use in southern Brazil. Agric Ecosyst Environ 115:237–247
Noller HF (1984) Structure of ribosomal RNA. Annu Rev Biochem 53:119–162
Noller HF (1991) Ribosomal RNA and translation. Annu Rev Biochem 60:191–227
Orr CH, Stewart CJ, Leifert C, Cooper JM, Cummings SP (2015) Effect of crop management and sample year on abundance of soil bacterial communities in organic and conventional cropping systems. J Appl Microbiol 119:208–214
Padmanabhan P, Padmanabhan S, DeRito C, Gray A, Gannon D, Snape JR, Tsai CS, Park W, Jeon C, Madsen EL (2003) Respiration of 13C-labeled substrates added to soil in the field and subsequent 16S rRNA gene analysis of 13C-labeled soil DNA. Appl Environ Microbiol 69:1614–1622
Paz-Ferreiro J, Fu S (2016) Biological indices for soil quality evaluation: perspectives and limitations. Land Degrad Dev 27:14–25
Pell M, Stenström J, Granhall U (2005) Soil respiration. In: Bloem J, Hopkins DW, Benedetti A (eds) Microbial methods for assessing soil quality, 1st edn. CABI, Wallingford, pp. 117–126
Peltoniemi K, Laiho R, Juottonen H, Kiikkila O, Makiranta P, Minkkinen K, Pennanen T, Penttila T, Sarjala T, Tuittila ES, Tuomivirta T, Fritze H (2015) Microbial ecology in a future climate: effects of temperature and moisture on microbial communities of two boreal fens. FEMS Microbiol Ecol 91:14
Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36:841–848
Perez-Osorio AC, Williamson KS, Franklin MJ (2010) Heterogeneous rpoS and rhlR mRNA levels and 16S rRNA/rDNA (rRNA Gene) ratios within Pseudomonas aeruginosa biofilms, sampled by laser capture microdissection. J Bacteriol 192:2991–3000
Pezzolla D, Marconi G, Turchetti B, Zadra C, Agnelli A, Veronesi F, Onofri A, Benucci GMN, Buzzini P, Albertini E, Gigliotti G (2015) Influence of exogenous organic matter on prokaryotic and eukaryotic microbiota in an agricultural soil: a multidisciplinary approach. Soil Biol Biochem 82:9–20
Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci U S A 109:10931–10936
Probert ME, Dimes JP, Keating BA, Dalal RC, Strong WM (1998) APSIM’s water and nitrogen modules and simulation of the dynamics of water and nitrogen in fallow systems. Agric Sys 56:1–28
Purahong W, Krueger D (2012) A better understanding of functional roles of fungi in the decomposition process: using precursor rRNA containing ITS regions as a marker for the active fungal community. Ann For Sci 69:659–662
Qu XH, Wang JG (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927
Ramirez-Villanueva DA, Bello-Lopez JM, Navarro-Noya YE, Luna-Guido M, Verhulst N, Govaerts B, Dendooven L (2015) Bacterial community structure in maize residue amended soil with contrasting management practices. Appl Soil Ecol 90:49–59
Rieder SR, Frey B (2013) Methyl-mercury affects microbial activity and biomass, bacterial community structure but rarely the fungal community structure. Soil Biol Biochem 64:164–173
Ros M, Pascual JA, Garcia C, Hernandez MT, Insam H (2006) Hydrolase activities, microbial biomass and bacterial community in a soil after long-term amendment with different composts. Soil Biol Biochem 38:3443–3452
Schimel J, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol. doi:10.3389/fmicb.2012.00348
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Segev E, Smith Y, Ben-Yehuda S (2012) RNA dynamics in aging bacterial spores. Cell 148:139–149
Stark S, Mannisto MK, Ganzert L, Tiirola M, Haggblom MM (2015) Grazing intensity in subarctic tundra affects the temperature adaptation of soil microbial communities. Soil Biol Biochem 84:147–157
Tardy V, Spor A, Mathieu O, Leveque J, Terrat S, Plassart P, Regnier T, Bardgett RD, van der Putten WH, Roggero PP, Seddaiu G, Bagella S, Lemanceau P, Ranjard L, Maron PA (2015) Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol Biochem 90:204–213
Todd-Brown KEO, Randerson JT, Post WM, Hoffman FM, Tarnocai C, Schuur EAG, Allison SD (2013) Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observations. Biogeosciences 10:1717–1736
Vetrovsky T, Baldrian P (2013) The variability of the 16S rRNA Gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One. doi:10.1371/journal.pone.0057923
Vogel C, Babin D, Pronk GJ, Heister K, Smalla K, Kogel-Knabner I (2014) Establishment of macro-aggregates and organic matter turnover by microbial communities in long-term incubated artificial soils. Soil Biol Biochem 79:57–67
Wakelin SA, Chu GX, Broos K, Clarke KR, Liang YC, McLaughlin MJ (2010) Structural and functional response of soil microbiota to addition of plant substrate are moderated by soil Cu levels. Biol Fertil Soils 46:333–342
Wang WJ, Dalal RC, Moody PW, Smith CJ (2003) Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biol Biochem 35:273–284
Wang YF, Hao YB, Cui XY, Zhao HT, CY X, Zhou XQ, ZH X (2014a) Responses of soil respiration and its components to drought stress. J Soils Sediments 14:99–109
Wang QK, Wang SL, He TX, Liu L, JB W (2014b) Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol Biochem 71:13–20
Wang QK, Wang YP, Wang SL, He TX, Liu L (2014c) Fresh carbon and nitrogen inputs alter organic carbon mineralization and microbial community in forest deep soil layers. Soil Biol Biochem 72:145–151
Widder S et al (2016) Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J. doi:10.1038/ismej.2016.45
Wittmann HG (1983) Architecture of prokaryotic ribosomes. Annu Rev Biochem 52:35–65
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74:5088–5090
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, and Eucarya. Proc Natl Acad Sci U S A 87:4576–4579
Xue D, Yao HY, Huang CY (2006) Microbial biomass, N mineralization and nitrification, enzyme activities, and microbial community diversity in tea orchard soils. Plant Soil 288:319–331
Yao S, Merwin IA, Bird GW, Abawi GS, Thies JE (2005) Orchard floor management practices that maintain vegetative or biomass groundcover stimulate soil microbial activity and alter soil microbial community composition. Plant Soil 271:377–389
Yuste JC, Baldocchi DD, Gershenson A, Goldstein A, Misson L, Wong S (2007) Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Chang Biol 13:2018–2035
Yuste JC, Penuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R, Pujol M, Sardans J (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Chang Biol 17:1475–1486
Yuste JC, Fernandez-Gonzalez AJ, Fernandez-Lopez M, Ogaya R, Penuelas J, Lloret F (2014) Functional diversification within bacterial lineages promotes wide functional overlapping between taxonomic groups in a Mediterranean forest soil. FEMS Microbiol Ecol 90:54–67
Zhang J, Wang F, Che RX, Wang P, Liu HK, Ji BM, Cui XY (2016) Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibetan alpine steppe. Sci Rep. doi:10.1038/srep23488
Zifcakova L, Vetrovsky T, Howe A, Baldrian P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol 18:288–301
Acknowledgments
This work was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB15010201), National Natural Science Foundations of China (41230750 and 31570518), and National Basic Research Program (2013CB956000). Rongxiao Che also received the Joint PhD Scholarship under the agreement between Griffith University and University of Chinese Academy of Sciences. We would like to express our sincere thanks to Damien Finn, Yongcui Deng, Li Tang, Qiushi Ning, and Linfeng Li for their insightful and constructive comments on improving the manuscript.
Author information
Affiliations
Corresponding authors
Additional information
Responsible editor: Hong Jie Di
Electronic supplementary material
ESM 1
(DOCX 238 kb)
Rights and permissions
About this article
Cite this article
Che, R., Wang, W., Zhang, J. et al. Assessing soil microbial respiration capacity using rDNA- or rRNA-based indices: a review. J Soils Sediments 16, 2698–2708 (2016). https://doi.org/10.1007/s11368-016-1563-6
Received:
Accepted:
Published:
Issue Date:
Keywords
- Soil microorganism
- Carbon cycle
- Microbial respiration
- rRNA
- Microbial activity