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Article

How Important Are the Relations between Vegetation Diversity and Bacterial Functional Diversity for the Functioning of Novel Ecosystems?

by
Gabriela Woźniak
1,
Monika Malicka
1,
Jacek Kasztowski
1,
Łukasz Radosz
1,
Joanna Czarnecka
2,*,
Jaco Vangronsveld
3,4 and
Dariusz Prostański
5
1
Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-032 Katowice, Poland
2
Department of Botany, Mycology and Ecology, Institute of Biological Sciences, Maria Curie-Skłodowska University, 20-033 Lublin, Poland
3
Department of Plant Physiology and Biophysics, Institute of Biological Sciences, Maria Curie-Skłodowska University, 20-033 Lublin, Poland
4
Centre for Environmental Sciences, Hasselt University, 3590 Diepenbeek, Belgium
5
KOMAG Institute of Mining Technology, 44-101 Gliwice, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(1), 678; https://doi.org/10.3390/su15010678
Submission received: 15 September 2022 / Revised: 18 December 2022 / Accepted: 22 December 2022 / Published: 30 December 2022
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Abstract

:
Understanding ecosystem development of post-mining areas requires observing the development of the plant and microbial communities. It is widely known that mutual interaction is important for both of these groups, and both benefit significantly. The aim of this study was to broaden the knowledge about the relation between the vegetation and functional diversity of bacterial communities in novel ecosystems of post-mining areas and to discuss the potential applicability of methods of studies of bacterial functional diversity in these ecosystems with special attention paid to the BIOLOG method. The functional diversity of microbial communities of five types of microhabitats of post-coal mining heap (Upper Silesia, Poland) was studied using the BIOLOG method. Four of them were covered by spontaneously developed vegetation (two dominated by grasses Calamagrostis epigejos and Poa compressa and two others by dicotyledonous species Daucus carota and Tussilago farfara). The results obtained for vegetated microhabitats were compared with the diversity of microbial communities from non-vegetated types of microhabitat. Our study confirmed that microbial functional diversity measured by the summed area under the curve for all substrates, the richness index, the Shannon-Wiener index and the evenness index mirrors aboveground vegetation diversity. All of these measures differ, especially between non-vegetated patches and grassland patches dominated by C. epigejos and P. compressa.

1. Introduction

Natural and semi-natural ecosystems are self-sustained, fundamental units in ecology, based on the cycles of matter and energy flow. The preliminary feature of each ecosystem is the species composition and functional diversity of primary producers. Plant species richness and functional identity significantly influence the above- and belowground ecosystem processes, particularly the decomposition of organic matter in all types of natural and semi-natural ecosystems [1,2,3,4,5]. Biodiversity in the taxonomic aspect and its influence on the whole ecosystem’s functioning are still of interest for current research and future challenges [2,6]. Species and functional diversity affect the use of resources, which forms the basis for the partitioning selection and complementarity concept in explaining the mechanisms and maintenance of biodiversity in ecosystems [7]. Studies of the global biodiversity scenarios are still developing and they prove that functional diversity affects decomposition processes in natural, semi-natural or experimental ecosystems [8,9,10,11].
For a long time, the study of biodiversity in various natural and semi-natural ecosystems on Earth focused on aboveground plant diversity. Fewer studies attempted to unravel and understand the importance of belowground biodiversity [12,13,14,15,16,17]. The above- and belowground elements of wetland and terrestrial ecosystems are linked via microorganisms colonizing the plant rhizosphere [18,19,20,21], endosphere and phyllosphere [22]. The autotrophic organisms, mostly plants, deposit litter and root exudates in soils providing a source of carbon and other nutrients for assemblages of decomposers. It is widely known that soil microbiota (with bacteria as its significant part), and their activity in decomposition are dependent on biochemical characteristics of soil organic matter (mostly plant remnants). They also play an essential role in the cycling of elements and providing inorganic nutrients for plant growth [6,23,24].
In the last decades the processes taking place during the Anthropocene revealed new aspects of natural phenomena. To a large extent, the growing area of habitats completely transformed by man with plant communities showing totally new species compositions (e.g., novel ecosystems established, with non-analogous species composition) not occurring in natural and semi-natural systems, generates many new research questions (Figure 1). Novel ecosystems develop in habitats that have been transformed so deeply (i.e., those where the crossing of the ecological threshold took place) that a return to the earlier state is no longer possible. In completely new habitat conditions, the assembly rules expressed by natural processes lead to the establishment of new, previously unknown, species assemblages and network of interactions [25,26,27].
Understanding the nature of novel ecosystems requires a study of their functional character. Apart from the identification of the non-analogous species composition of vascular plants, the biological analyses of the substrate (i.e., the activity of soil enzymes, functional diversity of microorganisms) as well as studies of species functional traits (morphological, biochemical or physiological) revealed that the adaptations that enable them to colonize harsh habitats are necessary. The harsh complex system of habitat conditions are caused by the lack of initial soils in the sites where the novel ecosystems develop. In many sites, the mineral material substrate without organic matter of granulometric structure (referred to as the soil substrate further in the text) is colonized by vascular plant species. It can be hypothesized that along with non-analogous plant species composition, the associated bacteria, fungi and animals will appear in unexpected arrangements, [28,29] leading to the establishment of a novel ecosystem. This is the reason for undertaking this complex study.
Apart from the complexity of microbial, plant combinations and abiotic conditions, and the limited understanding of these relations in natural and semi-natural ecosystems, human industrial activity brings completely new challenges. The extraction of mineral resources causes strong transformation of the landscape. The open cast mining and deposition of mineral material from deep mining change the land relief, remove the existing vegetation, and modify the soil structure and composition as well as hydrological conditions [30,31,32,33]. Specific chemical and physical properties of the mineral substrates are responsible for creating harsh conditions such as low water-holding capacity, poor nutrient concentrations, extreme pH and high temperatures [34,35]. In some sites, the changes of conditions and availability of resources are so fundamental that the given bio-geo-chemical habitat threshold is crossed, and then returning to the initial species composition is impossible. The habitats with vegetation appearing de novo are examples of novel ecosystems sensu (Hobbs et al. [27,36]). The spontaneous non-analogous plant species composition has been studied in coal mine heaps of novel ecosystems [15,16,17]. Studies have proven the existence of a wide variety of habitat conditions of coal mine heaps regarding moisture, granulometry and salinity, not to mention slope inclination, height, and aspect differences. Moreover, the habitat diversity within one coal mine heap is frequently much higher than that between two or more heaps. The great mosaic of microhabitats (e.g., moisture, granulometry, salinity) is reflected by the diverse vegetation patchiness [14,21,33]. The wide microhabitat variety is crucial in the single coal mine heap scale. The available studies of non-analogous species composition developed on coal mine heaps revealed that the novel ecosystems were significantly different from the surrounding non-industrial areas. The differences includes flora, fauna and associated saprophytic organisms, such as bacteria, fungi, mites (Mesostigmata group), saprophytic protists, etc., established as a result of the natural processes of colonization and recruitment in the novel habitats [25]. The non-analogous species composition of the novel ecosystems presents a self-sustaining system that develops without human intervention [31,36,37,38,39,40,41,42,43]. It also creates unusual opportunities to study the processes of primary succession in specific combinations of habitat conditions with special attention to substrates with low initial biological activity [44].

The Relation between the Diversity of Plant Species Composition of a Vegetation Cover and Bacterial Functional Diversity—Theory and Methods

The microbiota assemblages are significant drivers of soil organic matter decomposition processes [45,46]. The decomposition of dead organic matter depends on the metabolic activity of microorganisms and the biochemical parameters of the biomass [47,48]. The characteristics of the deposited biomass are controlled by factors such as humidity and temperature [48,49], soil properties [48,50] and vegetation type [51,52]. Due to the low homeostasis and high surface-to-volume ratio, the microorganisms respond quickly to changes in the environment [52]. Apart from the methods based on molecular assays such as the analysis of phospholipid fatty acids (PLFA) [53,54] or denaturing/temperature gradient gel electrophoresis (DGGE/TGGE) [55,56], the measurement of the physiological activity of microorganisms represents an important approach. The physiological activity of microorganisms allows for the study of functional characteristics of microbial communities [57]. The BIOLOG method is frequently used to compare the metabolic activity of heterotrophic microbial communities from the rhizosphere [58]. The intensity of the utilization of carbon substrates varies in different groups of microorganisms, which results in a given “metabolic fingerprint” of a microbial community [59,60,61,62,63,64,65].
The physiological profiles analyzed by means of multidimensional statistical methods allows for the comparison and assessment of similarity between microbial communities from different ecosystems and habitats. This method can be used for estimating changes in soil microbial communities that result from a long-term or a short exposure of the soil to the influence of extreme factors. The differences in metabolic response enable the evaluation of adverse changes in microbial communities between communities from transformed and reference areas. The parameters characterized by the BIOLOG method provide information about the changes in microbial community abundance. The community-level physiological profile (CLPP) allows for the disclosing of the effects on microbial functional diversity.
The aim of this study was to (1) broaden the knowledge about the relationship between vegetation and bacterial functional diversity in novel ecosystems of post-mining areas; and (2) discuss the potential applicability of methods of studies of bacteria functional diversity in novel ecosystems with special attention paid to the BIOLOG method.

2. Materials and Methods

2.1. Study Site Characteristics

The study site is situated in the central part of the Silesian Upland (southern Poland). This is a temperate climate area, with the highest mean temperature of 14–16 °C in July and an annual rainfall of 600–800 mm. The western winds are the most frequent in the region. The days with mist range from 30 to over 100, while the share of days with cloud cover is approximately 60–80% [66]. The fieldwork was conducted and the samples were collected from the “Makoszowy” coal mine heap (Zabrze, Sośnica; 50°16′22″ N, 18°44′43″ E); “Kostuchna” in Katowice (50°11′4″ N, 19°0′33″ E); and “Wesoła” in Mysłowice (50°10′28″ N, 19°5′44″ E). These coal mine heaps cover an area of approximately 170 hectares, and are located at an altitude of 310–339 m above the sea level. They are still active [66]. They are formed mainly from carboniferous rocks extracted from a depth of about 0.5 to 1 km below the surface and deposited at the spoil site [66]. New material is still transported to the top of the heap by a railway connecting the mine and the heap. The studied heaps are generally irregular and built of carboniferous gangue with unfavorable soil texture (mainly claystone and siltstone, sandstone, conglomerate, and coal shale) with admixtures of coal. Organisms colonizing the post-mineral excavation sites (Figure 2, Figure 3, Figure 4 and Figure 5), including the deep coal-mine heaps, are often subjected to extreme abiotic factors and conditions such as low water availability and retention, low nutrient availability, fast drying of the surface layer of substrate, low availability of organic matter, high temperature (reaching endogenous thermal activity) and high/variable salinity levels (crystallized salt can sometimes be observed). The substrate of coal mine heaps does not contain high concentrations of heavy metals and other dioxins in comparison to other post-industrial sites (e.g., lead and zinc spoil heaps) of anthropogenic origin [28,31,33,34,35,41,42]. Non-analogous species composition in these habitats has been formed in the process of primary succession.

2.2. Vegetation and Soil Sampling Methods

The studied vegetation patches represented a non-vegetated microhabitat and four vegetation types. Two groups of patches were chosen for detailed investigation: (i) those dominated by herbaceous species forb species (dicotyledons) (Daucus carota, Tussilago farfara); and (ii) those dominated by grass species (monocotyledons) (Calamagrostis epigejos, Poa compressa). Ten sample plots (circle, diameter 6 m) for each microhabitat type with plant cover and for non-vegetated patches were established to study the vegetation and functional diversity of the bacterial communities. The plots were separated at least 10 m from each other. All of the study plots were established on flat terrain (on the tops of spoil heaps) to unify the conditions between the plot exposure to sunlight and the susceptibility to erosion.
In the studied plots, the cover of vascular plants (estimated as cover for each species) was evaluated according to the scale as follows: 1, 2, 5, 10%, and the next at 10% intervals up to 100%.
To obtain material for analysis of bacterial functional diversity at each plot, the rhizosphere mineral material (substrate) was sampled from three points at a depth of 10 cm and mixed. The bulk samples were immediately transported to the laboratory and sieved with a 2 mm mesh sieve. The sieved material was put in polyurethane bags at 4 °C before the analysis was conducted.
Before the start of the procedure, both the needed equipment and the 0.85% saline solution were sterilized. A total of 10 g of dry soil was suspended in 90 mL of saline solution (dilution 10−1), incubated for 60 min on a shaker (120 rpm), and left to settle for 30 min. Next, 2 mL of the prepared soil suspension was transferred to 18 mL of fresh sterile saline solution (dilution 10−2). A total of 120 μL of solution was used to inoculate each of the 96 wells of the BIOLOG microplates. Immediately after inoculation (and every 24 h afterwards), the absorbance of soil suspension in the wells was measured at 590 nm using the BIOLOG MicroStation. The microplates were incubated at 22 °C for 5 days.
To measure and characterize the bacteria’s functional diversity, the study used the bacteria’s ability to diversify the intensity of digesting different sources of carbon used in the plates [67,68,69]. The following measurements were calculated: the summed area under the curve for all substrates (ΣAUC), the richness index (Rs), the Shannon-Wiener index (H’), and the evenness index (Eh) [70].
A statistical analysis was performed with Statistica 12 software. Assumptions for parametric tests were checked by the following methods: a normal probability plot followed by the Shapiro-Wilk test for normality of distribution and Levene’s test for the equity of variances. A non-parametric test (Kruskal-Wallis test with post-hoc test) was applied when it appeared that the assumptions were not fulfilled. In other cases, statistical significance of differences between mean values was tested with a one way ANOVA test along with the post-hoc Tukey’s test with the ω2 factor calculated additionally [71,72].
Discriminant analysis, after checking all the assumptions, was performed to verify if bacterial functional diversity follows the vegetation characteristics of studied novel ecosystems patches; and Statistica 12 software was again used [71,72].

3. Results

The characteristics of the vegetation are given in Table 1. The most abundant vegetation cover was founded in microhabitats dominated by C. epigejos, although the plant diversity there, measured by the mean number of species, was comparable to the diversity of the other vegetation types.
The BIOLOG-CLPP analysis revealed significant effects of plant species composition on the physiological diversity of microbial communities in the studied novel ecosystems. The highest values of total catabolic activity (∑AUC) were observed for the communities associated with C. epigejos. ∑AUC of microbial communities associated with T. farfara and non-vegetated patches were about 10 times lower than those of the microbial communities associated with the other plant species and differed significantly from the other vegetation types (Figure 6). The H’ index and the numbers of oxidized substrates (Rs) were the highest for the microbial communities associated with C. epigejos and P. compressa, but the observed differences were not so evident.
Discriminant analyses performed to check if the pattern of microbiome characteristics follows the differences in vegetation cover showed high levels of co-occurrence (Figure 7). Discrimination performed on the basis of microbiome characteristics covered the division of patches made on the basis of vegetation structure in 60% (90% in the case of non-vegetated patches, 70% in C. epigejos, 60% in D. carota and 40% in the case of P. compressa and T. farfara patches) and additionally showed high levels of similarity of microbiome characteristics between T. farfara and non-vegetated patches as well as in the case of grass-dominated vegetation types.

4. Discussion

The awareness that the development of stable ecosystems on degraded lands depends on complicated interactions among organisms, with the essential role played by plants and microbial assemblages, is steadily growing among scientists and practitioners. Understanding ecosystem development on post-mining areas requires following the development of both plant and microbial communities [73,74]. Mutual interaction is important for both groups, and both benefit significantly from it. Studies of the effect of the presence of T. farfara, an early colonizer of spoil heaps [75], on the development of the soil microbial community showed that plant roots increased microbial diversity and that biomass and roots influenced by the microbial community, including nitrogen fixators and arbuscular mycorrhizal fungi, were bigger with higher metabolic potential than the control [76,77,78,79]. In our study, measures characterizing bacterial functional diversity of non-vegetated patches and patches dominated by T. farfara did not differ significantly, and they were difficult to distinguish on the basis of the used data. The summed area under the curve for all substrates (∑AUC) and the richness index (Rs) were only slightly higher for T. farfara patches, but mean values did not differ significantly. More evident differences were noted between measurements calculated for the above mentioned two vegetation types and grassland patches (with C. epigejos and P. compressa) with significantly higher values. It is worth mentioning that the development of denser and more diverse grass-dominated vegetation types lasts longer than the development of sparse vegetation (the mean cover about 30%) dominated mostly by T. farfara, and that the time factor can significantly influence the development of the bacterial community. Studies across chronosequence plots spanning 54 years located in a brown coal mine spoil deposit area in the Czech Republic demonstrated an important role of bacteria in the initial stage of succession (soil development stage). Later bacterial communities changed less dynamically and followed changes in soil parameters rather than vegetation changes. The transformation of plant assemblages was mirrored by soil fungal communities to a higher extent [74]. The functional diversity of bacteria in the soil is significantly related to SOM in the soil. It affects the energy provision for microbial growth and enzyme production [54]. Most studies revealed positive correlations between microorganism activities and SOC and TN in human-disrupted areas [55,56,57,80]. Urbanová et al. [44] detected that during spontaneous succession on heaps after open-cast brown coal extraction, the presence of SOC and TN in the soil layer had a crucial influence on the activities of microorganisms. Wang et al. [81] revealed that the management of vegetation restoration impacted different carbon sources that influenced the functional diversity of the microbial community in sandy soils. For vegetated and unvegetated plots, it is possible that most of the carbon in the mineral material was related to organic matter of recent or geogenic origin [60,61]. Geogenic coal is not available to microorganisms, and therefore, despite the high content of organic carbon (10–18%), the substrate in the studied plots had low available carbon sources for microorganisms [62]. The lack of correlation between SOC and the activity of the microorganisms may be related to the small quantity of available carbon in the total pool of SOC in some studies [9,10,11].
Stefanowicz at al.’s [73] studies of microbial communities conducted using the BIOLOG method on 20 spoiled heaps in two age categories (5–10 and 15–25 years from the end of heaping) covered with three different vegetation types (T. farfara, C. epigejos, and Chamaenerion palustre as dominant species) also confirmed the importance of time and vegetation type for microbial community activity, bacterial functional richness and basal respiration [73]. All of these measurements were significantly higher for older heaps overgrown by all vegetation types in comparison to the control ones (bare ground in all heaps age categories).

The Constraints of Methods for Determining Functional Diversity

The BIOLOG tool allows for the assessment of the relationships between microbial communities of varied vegetation types and the land use type [63,82,83] under environmental stresses such as high salinity and high soil pH [84], pollution with hydrocarbons or heavy metals, or high temperatures [85,86,87,88,89,90]. The BIOLOG method enables the detection of even small variations in microbial functional communities, such as the responses of rhizosphere microorganisms to the plant’s aging [91]. Biodiversity decrease (e.g., bacterial diversity) is often caused by the extinction of species with narrow ecological requirements that are unable to face new environmental constraints [91,92,93].
The BIOLOG method enables one to obtain data about the microorganismal community based on the characteristic pattern of substrate utilization, since the microbial growth rate and substrate utilization reflect the microbial community function. In this respect, the results of the BIOLOG method application provide information about both the structure and function of the studied microbial communities [94]. The results display the potential and not the actual catabolic activity of a microorganismal community [55,62]. Different microorganisms have diverse abilities to utilize the substrates in the plates. The variety of the carbon substrates provided in the plates does not always reflect the substrates that are available to the microorganisms in the soil or the soil substratum environment. On the other hand, some bacterial species are unable to grow on plates because the crucial substrates are not present [95]. In some studies, complicated interactions between species, different nutrient requirements, and/or high microbial species diversity might cause ambiguities and problems. It can be very difficult to precisely assess which microorganisms used the substrates on the plate. It is possible that the fast-growing bacteria contribute the most to the reduction of the tetrazolium dye on bacterial plates, as they are adapted to high substrate concentrations [96,97]. The slow-growing bacteria, incapable of growing in conditions of high substrate concentrations, can sometimes remain undetected in the analysis [97]. Some bacteria are unable to reduce tetrazolium or are able to reduce it only in cases of high substrate concentrations [98,99]. Several studies confirmed that the physiological profile obtained on a plate reflects only a part of the microbial community diversity, and the conclusions about the function and structure of a whole bacteria assemblage must consider this. Taking the above into account, the results obtained by using the BIOLOG method provide data about the metabolic potential and functional diversity of the studied community which is able to metabolize actively and grow in plate conditions [90,100].
Physiological profiles of the microbial community can also be studied by the catabolic responses of the bacteria community to the addition of carbon substrates to separate soil samples. The measurement of CO2 efflux along with the direct measurements of CO2 production or O2 consumption reflects the catabolic response and assessment of respiration of the microbial community in the studied vegetation type. Sometimes the utilization of a particular substrate demands the presence of other organic compounds [101,102]. In this method, the soil extraction is not necessary, so inefficient extraction and inoculum density does not cause a problem. The microbial community activity is generally measured after 0–6 h and, different from the BIOLOG plates, relies on indigenous microbial activity rather than on microbial growth [101,103]. In the BIOLOG method, each substrate is in a separate well on the plate. The catabolic profiling approach enables one to avoid some problems documented in the BIOLOG plates method. High substrate concentrations, which can inhibit some species or cause substrate-accelerated death, are crucial [103,104].
Apart from the wide range of applications, the BIOLOG method generates some problems that need to be overcome. An example of such a problem is that the commonly used phosphate buffer for the extraction of the microorganisms is not an appropriate solution for the extraction of microorganismal communities from a soil with a high zinc content. Phosphate reacts with zinc and influences absorbance measurements, leading to unprecise readings [60,105,106]. Another problem that has to be taken into consideration is that physiological profiles of bacterial communities can provide different results depending on the used buffer type. A source of variation might be the fact that the phosphate buffer is also a source of nutrients for microorganisms [106]. The extraction method is essential when comparing physiological profiles. Special attention should be paid to the extraction of microbes from the soil. The extraction has to be effective enough to allow the preparation of a representative inoculum of the studied bacterial community [103,104].
An additional issue is the impact of the inoculum density standardization depending on the study aim. Inoculum density standardization is crucial when the study aims to estimate the dynamics of the microbial community composition [107]. It affects the average well colour development (AWCD) [89]. The suitable dilution of the soil solution fixes the number of microorganisms to a certain level. The standardized inoculum is inoculated into plate wells [108]. Unfortunately, soil solution dilution can lead to the loss of rare species in the studied community [89].
The analysis of average well colour development, AWCD, is the least sensitive to the impact of inoculum density [89]. Greater than ten-fold dilutions affect classification with AWCD to a significant extent. Additionally, the dependence of colour development on the number of bacterial cells in the inoculum is not apparent because of the complex nature of the metabolic response. The metabolic response is influenced by the competition and cooperation between the microorganisms [108].

5. Conclusions

The microorganism assemblages, along with plants, play a significant role in the development of sustainable ecosystems in post-excavated, transformed areas. Their composition depends on two main factors. The first one is the complex system of habitat conditions and the second is vegetation composition, both of which change significantly over time. Our study confirmed that microbial functional diversity measured by the summed area under the curve for all substrates, the richness index, the Shannon-Wiener index and the evenness index mirrors aboveground vegetation changes. All of these measures differ, especially between non-vegetated patches and grassland patches dominated by C. epigejos or P. compressa.
The data obtained by using the method allows us to evaluate the functional diversity of microbial communities developed in habitats overgrown by non-analogous plant species composition, e.g., in post mineral exploitation novel ecosystems, and enables us to compare it with data from non-transformed ecosystems. The results obtained by using this method can be used to perform an environmental risk assessment.

Author Contributions

Conceptualization, G.W., M.M. and J.K.; methodology, G.W., M.M. and J.K.; software, J.K.; validation, J.V., J.C. and D.P.; formal analysis, M.M. and J.K.; investigation, J.K., M.M.; resources, M.M. and Ł.R.; data curation, J.K.; writing—original draft preparation, G.W.; writing—review and editing, J.V., J.C. and D.P.; visualization, J.C., M.M., J.K. and Ł.R.; supervision, G.W. and J.C.; project administration, G.W.; funding acquisition, G.W. and D.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by The National Centre for Research and Development, Grant Number: TANGO1/268600/NCBR/2015 (INFOREVITA—System wspomagania rewitalizacji zwałowisk odpadów pogórniczych przy użyciu narzędzi geoinformatycznych/Geoinformatics tools a sup-porting system of coal mine spoil heaps reclamation); National Science Centre Poland, Grant Number: OPUS 2019/35/B/ST10/04141 (Linking soil substrate biogeochemical properties and spontaneous succession on post-mining areas: novel ecosystems in a human-transformed landscape); RFCS (Fundusz Badawczy Węgla I Stali), Grant Number: 847227 (SUMAD—Sustainable use of mining waste dumps); Institute of Biological Sciences, Maria Curie-Skłodowska University.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Agnieszka Błońska, Agnieszka Hutniczak for providing suggestions to the manuscript, and Wojciech Bierza for invaluable laboratory assistance during the previous study, which provided the results for the presented discussion and concepts in the presented study. We would like to thank the Mineral and Energy Economy Research Institute of the Polish Academy of Sciences for organizing the IMF and SEP that led to discussing and sharing ideas in this manuscript.

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Figure 1. Effects of the transformation of ecosystems.
Figure 1. Effects of the transformation of ecosystems.
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Figure 2. The organisms colonizing the post-mineral excavation sites subjected to extreme abiotic factors and conditions (“Wesoła” coal mine heap in Mysłowice; phot. G. Woźniak).
Figure 2. The organisms colonizing the post-mineral excavation sites subjected to extreme abiotic factors and conditions (“Wesoła” coal mine heap in Mysłowice; phot. G. Woźniak).
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Figure 3. The spontaneous occurrence of Phragmites australis on coal mine novel habitats (“Kostuchna” coal mine heap in Katowice; phot. G. Woźniak).
Figure 3. The spontaneous occurrence of Phragmites australis on coal mine novel habitats (“Kostuchna” coal mine heap in Katowice; phot. G. Woźniak).
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Figure 4. The range of hydrological conditions reflecting the micro-habitat diversity (“Makoszowy” coal mine heap in Zabrze; phot. G. Woźniak).
Figure 4. The range of hydrological conditions reflecting the micro-habitat diversity (“Makoszowy” coal mine heap in Zabrze; phot. G. Woźniak).
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Figure 5. The frequently spontaneously established patch with the domination of Tussilago farfara (“Wesoła” coal mine heap in Mysłowice; phot. G. Woźniak).
Figure 5. The frequently spontaneously established patch with the domination of Tussilago farfara (“Wesoła” coal mine heap in Mysłowice; phot. G. Woźniak).
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Figure 6. Results of the one-way ANOVA (a,b) and Kruskal-Wallis test (c,d) of measures characterizing bacteria functional diversity. (a) ΣAUC—summed area under the curve for all substrates; (b) Rs—richness index; (c) H′—Shannon-Wiener index; (d) Eh—evenness index; N = 10, post-hoc tests were performed (Tukey’s HSD test or U Mann-Whitney test; different letters indicate significantly different values, with p < 0.05. Vegetation type: Ce—C. epigejos dominated, Pc—P. compressa, Dc—Daucus carota, Tf—Tussilago farfara, NV—non vegetated patches.
Figure 6. Results of the one-way ANOVA (a,b) and Kruskal-Wallis test (c,d) of measures characterizing bacteria functional diversity. (a) ΣAUC—summed area under the curve for all substrates; (b) Rs—richness index; (c) H′—Shannon-Wiener index; (d) Eh—evenness index; N = 10, post-hoc tests were performed (Tukey’s HSD test or U Mann-Whitney test; different letters indicate significantly different values, with p < 0.05. Vegetation type: Ce—C. epigejos dominated, Pc—P. compressa, Dc—Daucus carota, Tf—Tussilago farfara, NV—non vegetated patches.
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Figure 7. Results of discrimination analysis made on four characteristics of microbiome (∑AUC, H’, Eh and Rs). Extra axes explain the influence of four given characteristics of the microbiome with the discriminative axes and values show the strength of the influence (range from −1.0 to 1.0). Axis 1 discriminates T. farfara and non-vegetated patches from the other vegetation types and the most important discriminating factor is ∑AUC. Axis 2 discriminates non-vegetated and C. epigejos patches from the other vegetation types and the main discriminating factor is the evenness index.
Figure 7. Results of discrimination analysis made on four characteristics of microbiome (∑AUC, H’, Eh and Rs). Extra axes explain the influence of four given characteristics of the microbiome with the discriminative axes and values show the strength of the influence (range from −1.0 to 1.0). Axis 1 discriminates T. farfara and non-vegetated patches from the other vegetation types and the most important discriminating factor is ∑AUC. Axis 2 discriminates non-vegetated and C. epigejos patches from the other vegetation types and the main discriminating factor is the evenness index.
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Table
Table 1. Characteristics of plant cover in four studied vegetation types.
Table 1. Characteristics of plant cover in four studied vegetation types.
Dominant SpeciesMean CoverAbundance of Dominant SpeciesSpecies Composition (Mean Number of Species; the Most Abundant Species)
Calamagrostis epigejos *73%10–80%12.8; Picris hieracioides, Oenothera sp., Senecio viscosus, Solidago gigantea, Poa compressa
Poa compressa *70%20–40%13.9; Leontodon autumnalis, Lotus corniculatus, Daucus carota, Plantago lanceolata, Achillea millefolium,
Medicago lupulina, Echium vulgare, Picris hieracioides, Calamagrostis epigejos
Daucus carota **54%5–30%12.8; Calamagrostis epigejos, Lotus corniculatus,
Hieracium piloselloides, Picris hieracioides, Matricaria maritima subs. inodora
Tussilago farfara **46%20–40%8.3; Calamagrostis epigejos, Daucus carota, Chamaenerion palustre, Hieracium piloselloides
Monocotyledons (grasses *) and dicotyledons (forbs **).
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Woźniak, G.; Malicka, M.; Kasztowski, J.; Radosz, Ł.; Czarnecka, J.; Vangronsveld, J.; Prostański, D. How Important Are the Relations between Vegetation Diversity and Bacterial Functional Diversity for the Functioning of Novel Ecosystems? Sustainability 2023, 15, 678. https://doi.org/10.3390/su15010678

AMA Style

Woźniak G, Malicka M, Kasztowski J, Radosz Ł, Czarnecka J, Vangronsveld J, Prostański D. How Important Are the Relations between Vegetation Diversity and Bacterial Functional Diversity for the Functioning of Novel Ecosystems? Sustainability. 2023; 15(1):678. https://doi.org/10.3390/su15010678

Chicago/Turabian Style

Woźniak, Gabriela, Monika Malicka, Jacek Kasztowski, Łukasz Radosz, Joanna Czarnecka, Jaco Vangronsveld, and Dariusz Prostański. 2023. "How Important Are the Relations between Vegetation Diversity and Bacterial Functional Diversity for the Functioning of Novel Ecosystems?" Sustainability 15, no. 1: 678. https://doi.org/10.3390/su15010678

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