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. 2025 Jan 6:15:1523084.
doi: 10.3389/fmicb.2024.1523084. eCollection 2024.

Iron-oxidizing microorganisms affect the iron-bound organic carbon in the subsoil of alpine grassland during the thawing of seasonal frozen soil

Yuxin Tian  1 , Maidinuer Abulaizi  1 , Zailei Yang  2 , Tianle Kou  2 , Yuanbin Jia  2 , Yunpeng Hu  2 , Mo Chen  1   2   3 , Hongtao Jia  1   2   3
Affiliations

Iron-oxidizing microorganisms affect the iron-bound organic carbon in the subsoil of alpine grassland during the thawing of seasonal frozen soil

Yuxin Tian et al. Front Microbiol. .

Abstract

Iron (Fe) minerals possess a huge specific surface area and high adsorption affinity, usually considered as "rust tanks" of organic carbon (OC), playing an important role in global carbon storage. Microorganisms can change the chemical form of Fe by producing Fe-chelating agents such as side chains and form a stable complex with Fe(III), which makes it easier for microorganisms to use. However, in seasonal frozen soil thawing, the succession of soil Fe-cycling microbial communities and their coupling relationship with Fe oxides and Fe-bound organic carbon (Fe-OC) remains unclear. We characterized changes in the Fe phase, Fe-OC, Fe-oxidizing bacteria (FeOB), and Fe-reducing bacteria (FeRB) in the subsoil and analyzed the microbial mechanism underlying Fe-OC changes in alpine grassland by constructing a composite structural equation model (SEM). We found that the Fe(III) content consistently exceeded that of Fe(II). Among the three types of Fe oxides, organically complex Fe (Fep) decreased from 2.54 to 2.30 g·kg-1, whereas the opposite trend was observed for poorly crystalline Fe (Feo). The Fe-OC content also decreased (from 10.31 to 9.47 g·kg-1; p < 0.05). Fe-cycling microorganisms were markedly affected by the thawing of frozen soil (except FeRB). Fep and Feo directly affected changes in Fe-OC. Soil moisture (SM) and FeOB were significant indirect factors affecting Fe-OC changes. Freeze-thaw changes in the subsoil of alpine grassland in Central Asia significantly affected FeOB and Fe oxides, thus affecting the Fe-OC content. To the best of our knowledge, this was the first study to examine the influence of Fe-cycling microorganisms on the Fe phase and Fe-OC in the soil of alpine grassland in Central Asia. Overall, our findings provide scientific clues for exploring the biogeochemical cycle process in future climate change.

Keywords: Fe-bound organic carbon; Fe-cycling functional genes; Fe-cycling microorganisms; alpine grassland; thawing of seasonal frozen soil.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Effects of seasonal frozen soil thawing on ST, SM, and Fe phase. Different letters indicate significant differences between groups at the 0.05 level. ST, soil temperature; SM, soil moisture; Fed, free Fe oxides; Feo, poorly crystalline Fe oxides; Fep, organically complexed Fe oxides; Fe-OC, Fe-bound organic carbon.; M2, deep freezing period (early February); M4, initial thawing period (early April); M6, complete thawing period (early June).
Figure 2
Figure 2
(a)Temporal variation characteristics of β diversity in FeOB community; (b) Temporal variation characteristics of FeOB community composition;(c) Temporal variation characteristics of β diversity in FeRB community; (d) Temporal variation characteristics of FeRB community composition. * and ** indicate significance at the 0.05 and 0.01 levels, respectively. The points in NMDS represent samples, and different colors represent the information of the group to which the samples belong. The distance between points in the same group indicates the degree of dispersion of samples. M2, deep freezing period (early February); M4, initial thawing period (early April); M6, complete thawing period (early June).
Figure 3
Figure 3
(a) RDA analysis was performed with FeOB community as the response variable and ST, SM, Fe(III), Fe(II), Fed, Feo, Fep, and Fe-OC as the explanatory variables; (b) Correlation analysis between FeOB community and examining factors; (c) RDA analysis was performed with FeRB community as the response variable and ST, SM, Fe(III), Fe(II), Fed, Feo, Fep, and Fe-OC as the explanatory variables; (d) Correlation analysis between FeRB community and examining factors. *, **, and *** indicate significance at the 0.05, 0.01, and 0.001 levels, respectively. ST, soil temperature; SM, soil moisture; Fed, free Fe oxides; Feo, poorly crystalline Fe oxides; Fep, organically complexed Fe oxides; Fe-OC, Fe-bound organic carbon; M2, deep freezing period (early February); M4, initial thawing period (early April); M6, complete thawing period (early June).
Figure 4
Figure 4
(a)Temporal variation characteristics of β diversity in Fe oxidation genes; (b) Temporal variation characteristics of Fe oxidation genes composition; (c) Temporal variation characteristics of β diversity in Fe reduction genes; (d) Temporal variation characteristics of Fe reduction genes composition. * and ** indicate significance at the 0.05 and 0.01 levels, respectively. The points in NMDS represent samples, and different colors represent the information of the group to which the samples belong. The distance between points in the same group indicates the degree of dispersion of samples. M2, deep freezing period (early February); M4, initial thawing period (early April); M6, complete thawing period (early June).
Figure 5
Figure 5
(a) RDA analysis was performed with Fe oxidation genes as the response variables and ST, SM, Fe(III), Fe(II), Fed, Feo, Fep, and Fe-OC as the explanatory variables; (b) Correlation analysis between Fe oxidation genes and examining factors; (c) RDA analysis was performed with Fe reduction genes as the response variables and ST, SM, Fe(III), Fe(II), Fed, Feo, Fep, and Fe-OC as the explanatory variables; (d) Correlation analysis between Fe reduction genes and examining factors. *, **, and *** indicate significance at the 0.05, 0.01, and 0.001 levels, respectively. ST, soil temperature; SM, soil moisture; Fed, free Fe oxides; Feo, poorly crystalline Fe oxides; Fep, organically complexed Fe oxides; Fe-OC, Fe-bound organic carbon; M2, deep freezing period (early February); M4, initial thawing period (early April); M6, complete thawing period (early June).
Figure 6
Figure 6
Indirect and direct effects of factors affecting Fe-OC. SM, soil moisture; Fed, free Fe oxides; Feo, poorly crystalline Fe oxides; Fep, organically complexed Fe oxides; Fe-OC, Fe-bound organic carbon. Fe oxidation genes, FeOB, FeRB, Fe reduction genes, Fe, and Fe oxide variables were divided into compound variables. The numbers adjacent to the measured variables are their coefficients with the composite variables. The number adjacent to the arrow is the path coefficient, which is the direct standardized effect. The dashed lines indicate the significance of the relationship. The standardized effect of comprehensive variables on Fe-OC is shown in the marginal and conditional R2, which represents the proportion of variance explained by all predictive variables. The relationship between the residual variables that measure the predictor is not shown.
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