Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing

Freshwater ecosystems are critical but fragile environments directly affecting society and its welfare. However, our understanding of genuinely freshwater microbial communities, constrained by our capacity to manipulate its prokaryotic participants in axenic cultures, remains very rudimentary. Even the most abundant components, freshwater Actinobacteria, remain largely unknown. Here, applying deep metagenomic sequencing to the microbial community of a freshwater reservoir, we were able to circumvent this traditional bottleneck and reconstruct de novo seven distinct streamlined actinobacterial genomes. These genomes represent three new groups of photoheterotrophic, planktonic Actinobacteria. We describe for the first time genomes of two novel clades, acMicro (Micrococcineae, related to Luna2,) and acAMD (Actinomycetales, related to acTH1). Besides, an aggregate of contigs belonged to a new branch of the Acidimicrobiales. All are estimated to have small genomes (approximately 1.2 Mb), and their GC content varied from 40 to 61%. One of the Micrococcineae genomes encodes a proteorhodopsin, a rhodopsin type reported for the first time in Actinobacteria. The remarkable potential capacity of some of these genomes to transform recalcitrant plant detrital material, particularly lignin‐derived compounds, suggests close linkages between the terrestrial and aquatic realms. Moreover, abundances of Actinobacteria correlate inversely to those of Cyanobacteria that are responsible for prolonged and frequently irretrievable damage to freshwater ecosystems. This suggests that they might serve as sentinels of impending ecological catastrophes.     

Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence

It is uncertain whether the same ecological forces that structure plant and animal communities also shape microbial communities, especially those residing in soil. We sought to uncover the relative importance of present-day environmental characteristics, climatic variation, and historical contingencies in shaping soil actinobacterial communities in a long-term chronosequence. Actinobacteria communities were characterized in surface soil samples from four replicate forest stands with nearly identical edaphic and ecological properties, which range from 9500 to 14,000 years following glacial retreat in Michigan. Terminal restriction fragment length polymorphism (TRFLP) profiles and clone libraries of the actinobacterial 16S rRNA gene were constructed in each site for phenetic and phylogenetic analysis to determine whether dispersal limitation occurred following glacial retreat, or if community composition was determined by environmental heterogeneity. At every level of examination, actinobacterial community composition most closely correlated with distance, a surrogate for time, than with biogeochemical, plant community, or climatic characteristics. Despite correlation with leaf litter C:N and annual temperature, the significant and consistent relationship of biological communities with time since glacial retreat provides evidence that dispersal limitation is an ecological force structuring actinobacterial communities in soil over long periods of time.     

Planktonic actinobacterial diversity along a salinity gradient of a river and five lakes on the Tibetan Plateau

The diversity and community structure of planktonic Actinobacteria in a freshwater river and five fresh/saline/hypersaline lakes on the Tibetan Plateau, China were investigated with a combination of geochemical and 16S rRNA gene phylogenetic analyses. A total of 387 actinobacterial 16S rRNA gene clones were sequenced, and they could be classified into Actinobacteridae, Acidimicrobidae, and unclassified Actinobacteria. The Actinobacteridae sequences were distributed into five suborders (e.g., Corynebacterineae, Frankineae, Micrococcineae, Propionibacterineae, and Streptosporangineae) and unclassified Actinobacteridae. Some actinobacterial members (specifically Micrococcineae) were present in a wide range of salinities (from freshwater to NaCl saturation). Statistical analysis showed that salinity and salinity-related environmental variables (such as ions and total nitrogen) significantly (r > 0.5; P < 0.05) influenced the distribution of planktonic actinobacterial community in the investigated aquatic biotopes. Our data have implications for a better understanding of the distribution of Actinobacteria in high-elevation lakes.     

Modulation of respiratory metabolism in response to nutrient changes along a soil chronosequence

Laboratory studies indicate that plant respiratory efficiency may decrease in response to low nutrient availability due to increased partitioning of electrons to the energy‐wasteful alternative oxidase (AOX); however, field confirmation of this hypothesis is lacking. We therefore investigated plant respiratory changes associated with succession and retrogression in soils aged from 10 to 120 000 years along the Franz Josef soil chronosequence, New Zealand. Respiration rates and electron partitioning were determined based on oxygen isotopic fractionation. Leaf structural traits, foliar nutrient status, carbohydrates and species composition were measured as explanatory variables. Although soil nutrient levels and species composition varied by site along the chronosequence, foliar respiration across all sites and species corresponded strongly with leaf nitrogen concentration (r² = 0.8). In contrast, electron partitioning declined with increasing nitrogen/phosphorus (r² = 0.23) and AOX activity correlated with phosphorus (r² = 0.64). Independently, total respiration was further associated with foliar Cu, possibly linked to its effect on AOX. Independent control of AOX and cytochrome pathway activities is also discussed. These responses of plant terminal respiratory oxidases – and therefore respiratory carbon efficiency – to multiple nutrient deficiencies demonstrate that modulation of respiratory metabolism may play an important role in plant responses to nutrient gradients.     

Actinobacterial Diversity in Microbial Mats of Five Hot Springs in Central and Central-Eastern Tibet,China

The diversity and community composition of Actinobacteria in microbial mats of five Tibetan hot springs (temperatures 26°C to 81°C) and a sympatric soil were investigated with 16S rRNA gene phylogentic analysis. A total of 278 clones were obtained. The actinobacterial communities in the Tibetan hot springs were diverse, and most of the retrieved clones were affiliated with Actinobacteridae, Acidimicrobidae, and unclassified Actinobacteria. The Actinobacteridae sequences were distributed into seven suborders (e.g., Frankineae, Corynebacterineae, Micromonosporineae, Pseudonocardineae, Propionibacterineae, Micrococcineae, and Actinomycineae) and unclassified Actinobacteridae. The actinobacterial composition varied among different hot springs. Statistical analysis showed that the actinobacterial diversity in the investigated Tibetan hot springs was not significantly correlated with temperature, suggesting that temperature is not a key factor in shaping the actinobacterial diversity in hot springs.     

Microbial Community Succession in an Unvegetated,Recently Deglaciated Soil

Primary succession is a fundamental process in macroecosystems; however, if and how soil development influences microbial community structure is poorly understood. Thus, we investigated changes in the bacterial community along a chronosequence of three unvegetated, early successional soils (∼20-year age gradient) from a receding glacier in southeastern Peru using molecular phylogenetic techniques. We found that evenness, phylogenetic diversity, and the number of phylotypes were lowest in the youngest soils, increased in the intermediate aged soils, and plateaued in the oldest soils. This increase in diversity was commensurate with an increase in the number of sequences related to common soil bacteria in the older soils, including members of the divisions Acidobacteria, Bacteroidetes, and Verrucomicrobia. Sequences related to the Comamonadaceae clade of the Betaproteobacteria were dominant in the youngest soil, decreased in abundance in the intermediate age soil, and were not detected in the oldest soil. These sequences are closely related to culturable heterotrophs from rock and ice environments, suggesting that they originated from organisms living within or below the glacier. Sequences related to a variety of nitrogen (N)-fixing clades within the Cyanobacteria were abundant along the chronosequence, comprising 6–40% of phylotypes along the age gradient. Although there was no obvious change in the overall abundance of cyanobacterial sequences along the chronosequence, there was a dramatic shift in the abundance of specific cyanobacterial phylotypes, with the intermediate aged soils containing the greatest diversity of these sequences. Most soil biogeochemical characteristics showed little change along this ∼20-year soil age gradient; however, soil N pools significantly increased with soil age, perhaps as a result of the activity of the N-fixing Cyanobacteria. Our results suggest that, like macrobial communities, soil microbial communities are structured by substrate age, and that they, too, undergo predictable changes through time.     

Primary Succession of Soil Rotifers in Clays of Brown Coal Post‐Mining Dumps

Changes in rotifer soil communities along a primary succession chronosequence was studied on brown coal post mining areas near Sokolov, NW part of the Czech Republic. The chronosequence of unreclaimed plots was 2, 11, 14, 20, 43 years old. The rotifers were extracted from soil samples using a modification of the Baermann funnel method with combined light and temperature gradients. In total, 34 taxa of soil rotifers were identified throughout the study. The most common species were Encentrum arvicola, Adineta vaga, A. steineri, Habrotrocha rosa, H. elegans, H. filum, Macrotrachela quadricornifera and M. nana. Rotifer abundance varied from 4 ± 2 · 10³ to 516 ± 488 · 10³ individuals m^–2. Species number per sample increased with age of the plot (r = 0.45, P = 0.003). The most important environmental variables which significantly affected rotifer community were wood cover, sodium concentration and age of the plot. Pioneer plant species occupied 2 and 11 year old plots, 14–20 year old plots were covered by Salix caprea shrubs and a forest formed by Betula pendula and Populus tremuloides developed on the 43 year old plot. Some species were ubiquitous and present throughout the chronosequence (Macrotrachela quadricornifera). Among the pioneer species were Encentrum incisum, Habrotrocha rosa and Macrotrachela papillosa, 14–20 years old plots were preferred by Adineta vaga, E. arvicola, H. filum and M. nana, while the oldest plot was dominated by Adineta steineri and Encentrum mucronatum. (© 2011 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

“Preferential” ammonium uptake by sugarcane does not increase the <Superscript>15</Superscript>N recovery of fertilizer sources

Aims

Human activities can dramatically alter natural plant communities which, after disturbance cessation, undergo secondary succession. In arid environments plant succession is quite slow, and its link to the carbon (C) cycle is not well known. We assessed changes in C balance on a semiarid plant community along a chronosequence spanning ca. 100 years after land abandonment in an arid environment in SE Spain to examine temporal changes in C following human disturbance.

Methods

We selected 5 individuals of the dominant plant species along five plant community stages differing in the time since land abandonment occurred, and we used a closed-chamber infrared gas analyzer method to estimate the contribution of whole plants and bare soil to community C exchange. We estimated CO₂ fluxes for each plant community stage and calculated temporal differences along the chronosequence.

Results

Plant community composition and plant cover changed throughout the chronosequence. Carbon balance was related to changes in plant photosynthesis and plant and soil respiration along the chronosequence. Overall, community C exchange shifted from source to sink as plant colonization progressed. It took 65 years for the system to recover the equivalent C sink capacity of the undisturbed site.

Conclusions

Recovery of arid plant communities after land abandonment may enhance long-term C sequestration and significantly contribute to C balance at the global level.

     

Ectomycorrhiza communities of red oak (<Emphasis Type="BoldItalic">Quercus rubra</Emphasis> L.) of different age in the Lusatian lignite mining district,East Germany

Ectomycorrhizal (ECM) communities were assessed on a 720 m² plot along a chronosequence of red oak (Quercus rubra) stands on a forest reclamation site with disturbed soil in the lignite mining area of Lower Lusatia (Brandenburg, Germany). Adjacent to the mining area, a red oak reference stand with undisturbed soil was investigated reflecting mycorrhiza diversity of the intact landscape. Aboveground, sporocarp surveys were carried out during the fruiting season in a 2-week interval in the years 2002 and 2003. Belowground, ECM morphotypes were identified by comparing sequences of the internal transcribed spacer regions from nuclear rDNA with sequences from the GenBank database. Fifteen ECM fungal species were identified as sporocarps and 61 belowground as determined by morphological/anatomical and molecular analysis of their ectomycorrhizas. The number of ECM morphotypes increased with stand age along the chronosequence. However, the number of morphotypes was lower in stands with disturbed soil than with undisturbed soil. All stands showed site-specific ECM communities with low similarity between the chronosequence stands. The dominant ECM species in nearly all stands was Cenococcum geophilum, which reached an abundance approaching 80% in the 21-year-old chronosequence stand. Colonization rate of red oak was high (>95%) at all stands besides the youngest chronosequence stand where colonization rate was only 15%. This supports our idea that artificial inoculation with site-adapted mycorrhizal fungi would enhance colonization rate of red oak and thus plant growth and survival in the first years after outplanting.     

Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments

The microbiomes of rhizocompartments (nodule endophytes, root endophytes, rhizosphere and root zone) in soya bean and alfalfa were analysed using high‐throughput sequencing to investigate the interactions among legume species, microorganisms and soil types. A clear hierarchical filtration of microbiota by plants was observed in the four rhizocompartments – the nodule endosphere, root endosphere, rhizosphere and root zone – as demonstrated by significant variations in the composition of the microbial community in the different compartments. The rhizosphere and root zone microbial communities were largely influenced by soil type, and the nodule and root endophytes were primarily determined by plant species. Diverse microbes inhabited the root nodule endosphere, and the corresponding dominant symbiotic rhizobia belonged to Ensifer for alfalfa and Ensifer–Bradyrhizobium for soya bean. The nonsymbiotic nodule endophytes were mainly Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. The variation in root microbial communities was also affected by the plant growth stage. In summary, this study demonstrated that the enrichment process of nodule endophytes follows a hierarchical filtration and that the bacterial communities in nodule endophytes vary according to the plant species.     

干旱区高寒湿地逆行演替下土壤微生物群落结构的研究

【目的】探究高寒湿地逆行演替对土壤性质与微生物群落结构的影响。【方法】以新疆巴音布鲁克天鹅湖高寒湿地为研究对象,依托逆行演替典型样带(沼泽-沼泽化草甸-草甸),利用高通量测序技术分析各演替区土壤微生物群落结构。【结果】高寒湿地逆行演替改变了土壤微生物在分类操作单元(operational taxonomic unit,OTU)水平上的物种组成,致使草甸区的微生物ACE、Chao1、Simpson、Shannon多样性指数显著低于沼泽区和沼泽化草甸区(P<0.05);随着演替发生,变形菌门(Proteobacteria)、酸杆菌门(Acidobacteria)、拟杆菌门(Bacteroidetes)、子囊菌门(Ascomycota)的相对丰度均减少,放线菌门(Actinobacteria)、芽单胞菌门(Gemmatimonadetes)、担子菌门(Basidiomycota)、被孢霉门(Mortierellomycota)的相对丰度增加;主坐标法分析(principal coordinates analysis,PCoA)排序分析显示,土壤微生物群落在各逆行演替都出现不同程度的离散...     

Bacterial succession during 500?years of soil development under agricultural use

Soil bacterial succession under intensive anthropogenic disturbances is not well known. Using terminal restriction fragment length polymorphisms and 454 pyrosequencing of 16S rRNA genes, this study investigated how soil bacterial diversity and community structure changed under two agricultural land uses (paddy rice and upland cropping) in relation to soil development along a 500-year chronosequence created by intermittent reclamation of estuarine salt marshes. Multivariate analysis revealed orderly changes in soil physicochemical properties and bacterial community structure with time, confirming the occurrence of soil development and bacterial succession. Patterns of soil development and bacterial succession resembled each other, with recent land uses affecting their trajectories but not the overall direction. Succession of bacterial community structure was mainly associated with changes in ??-Proteobacteria and Verrucomicrobia. Two stages of bacterial succession were observed, a dramatic-succession stage during the first several decades when bacterial diversity increased evidently and bacterial community structure changed rapidly, and a long gradual-succession stage that lasted for centuries. Canonical correspondence analysis identified soil Na⁺, potentially mineralizable nitrogen, total phosphorous, and crystallinity of iron oxyhydrates as potential environmental drivers of bacterial succession. To conclude, orderly succession of soil bacterial communities occurred along with the long-term development of agroecosystems, which in turn was associated with soil physicochemical changes over time.     

Soil animal communities at five succession stages in the litter of the evergreen broad-leaved forest in Tiantong, China

Soil animals are abundant in forest litter layer, but little attention has been paid to the vertical distribution of community structure of soil animals in the layers at different plant community succession stages. The forest litter layer can be divided into fresh litter layer (L), fermentation layer (F) and humus layer (H), which may represent different litter decomposition stages. The aim of the study is to ascertain the vertical distribution features of soil animal communities among the three litter layers and the change in the succession process of the Evergreen Broad-Leaved Forest (EBLF) in Tiantong, Zhejiang Province, China. Soil animal communities in the five plant communities at different succession stages were investigated during the 2003 winter. Soil animals, which were collected by using Tullgren funnels, amounted to a total of 13 381 individuals falling into 2 phyla, 8 classes and 20 orders. The dominant groups were Acarina and Collembola, accounting for 94.24% of the total individuals, with the number of Acarina individuals 7.66 times than that of Collembola. The common group was Diptera. The results indicated that there was a distinctive vertical distribution of the soil animal communities in the forest litter layer, but it differed from that in soil below the litter layer. In contrast to those in the soil, the soil animals in the litter layer generally tended to increase in both group abundance and density from the top fresh litter layer to the bottom humus layer. Altogether 19 groups and 59.03% of total individuals were found in the bottom layer, while only 8 groups and 5.35% of the total individuals in the top. Moreover, there were some variations in the distribution of the soil animals at different plant succession stages. 85.19% of Homoptera and 100% of Symphyla were found in the litter layer at the climax succession stage, while 75.61% of Thysanoptera at the intermediate succession stage. Therefore, these groups might be seen as indicative groups. The total numbers of soil animal groups and individuals in the litter layers greatly changed in the succession process of the EBLF. They both were greatest at the climax, moderate at the intermediate and smallest at the primary succession stage. However, the main soil animal groups in the litter at the different succession stages were essentially the same. They were Acarina, Collembola, Diptera and Lepidoptera. Although similarity analysis revealed that the soil animal communities in the litter at the intermediate succession stage were most similar to those at the climax succession stage, they differed greatly from each other in the Shannon-Wiener diversity index. The Shannon-Wiener index was highest at the climax succession stage and lowest at the intermediate succession stage. Finally, the paper discusses the following three questions: the role of soil animals as indicators for plant community succession; the role of different soil animal groups in the litter decomposition at different stages; and the major factors affecting the composition and distribution of soil animals in the litter. This paper provides a new perspective for the research on the succession mechanism of plant communities and the decomposition functions of soil animals. __________ Translated from Acta Ecologica Sinica, 2005, 25 (3) [译自: 生态学报, 2005,25(3)]     

Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils

Early community assembly of soil microbial communities is essential for pedogenesis and development of organic legacies. We examined fungal and bacterial successions along a well‐established temperate glacier forefront chronosequence representing ~70 years of deglaciation to determine community assembly. As microbial communities may be heavily structured by establishing vegetation, we included nonvegetated soils as well as soils from underneath four plant species with differing mycorrhizal ecologies (Abies lasiocarpa, ectomycorrhizal; Luetkea pectinata, arbuscular mycorrhizal; Phyllodoce empetriformis, ericoid mycorrhizal; Saxifraga ferruginea, nonmycorrhizal). Our main objectives were to contrast fungal and bacterial successional dynamics and community assembly as well as to decouple the effects of plant establishment and time since deglaciation on microbial trajectories using high‐throughput sequencing. Our data indicate that distance from glacier terminus has large effects on biomass accumulation, community membership, and distribution for both fungi and bacteria. Surprisingly, presence of plants rather than their identity was more important in structuring bacterial communities along the chronosequence and played only a very minor role in structuring the fungal communities. Further, our analyses suggest that bacterial communities may converge during assembly supporting determinism, whereas fungal communities show no such patterns. Although fungal communities provided little evidence of convergence in community structure, many taxa were nonrandomly distributed across the glacier foreland; similar taxon‐level responses were observed in bacterial communities. Overall, our data highlight differing drivers for fungal and bacterial trajectories during early primary succession in recently deglaciated soils.     

Vegetation succession at the abandoned Ogushi sulfur mine, central Japan

We surveyed plant community development at the abandoned Ogushi sulfur mine. We found seven communities dominated by the following respective species: Deschampsia flexuosa, Miscanthus sinensis, shrub willow, Gaultheria miqueliana–Betula ermanii, Sasa senanensis–Betula ermanii, willow–Betula ermanii, and Sasa kurilensis–Abies veitchii. We examined the succession of these communities, in which younger communities of low height and ground cover contained seedlings of the successive communities that were taller and had higher ground cover. To understand the development of these different communities, we surveyed damage from mining pollution and effects of immature soils formed by landslides. The average pH (H₂O) was 4.12, and aluminum concentrations were not sufficiently high to damage plant growth, except in areas where sulfur had been mined. The organic carbon and nitrogen content in soil samples were very low because of a delay in soil development caused by a large landslide in 1937. Hence, succession was positively correlated with the soil development stage. The delay in soil development after a large landslide influenced the seven successional steps of the plant communities, but mineral poisons at the abandoned Ogushi sulfur mine had no effect on succession.     

Actinobacterial community dynamics in long term managed grasslands

Palace Leas, a long-term experiment at Cockle Park Farm, Northumberland, UK was established in winter 1896–1897 since when the 13 plots have received regular and virtually unchanged mineral fertiliser and farm yard manure inputs. Fertilisers have had a profound impact on soil pH with the organically fertilised plots showing a significantly higher pH than those receiving mineral fertiliser where ammonium sulphate has led to soil acidification. Here, we investigate the impact of organic and mineral fertilisers on the actinobacterial community structure of these soils using terminal restriction fragment length polymorphism (T-RFLP) and 16S rRNA gene analysis. To differentiate fertiliser effects from seasonal variation, soils were sampled three times over one growing season between May and September 2004 and January 2005. Community profiles obtained using T-RFLP were analysed using multivariate statistics to investigate the relationship between community structure, seasonality and fertiliser management. Soil pH was shown to be the most significant edaphic factor influencing actinobacterial communities. Canonical correspondence analysis, used to investigate the relationship between the 16S rRNA gene community profiles and the environmental parameters, showed that actinobacterial communities also responded to soil water content with major changes evident over the summer months between May and September. Quantitative PCR of the actinobacterial and fungal 16S and 18S rRNA genes, respectively suggested that fungal rRNA gene copy numbers were negatively correlated (P = 0.0131) with increasing actinobacterial signals. A similar relationship (P = 0.000365) was also evident when fatty acid methyl esters indicative of actinobacterial biomass (10-methyloctadecanoic acid) were compared with the amounts of fungal octadecadienoic acid (18:2ω9,12). These results show clearly that soil pH is a major driver of change in actinobacterial communities and that genera such as Arthrobacter and Micrococcus are particularly abundant in soils receiving organic inputs whilst others such as Streptomyces, Acidimicrobium and Actinospica are more prevalent in acid soils. The importance of these findings in terms of fungal abundance and potential disease suppression are discussed.     

Ecological Strategies of Soil Microbial Communities under Plants of Meadow Ecosystems

Dominant growth strategies of soil microbial communities of mown and unmown meadows were assessed with respect to the constants of saturation and maximal specific growth rate of microorganisms. The microbial community of mown-meadow soil was characterized by a greater biomass and activity due to prevalence of microorganisms with the r strategy, compared to the microbial community of unmown-meadow soil. In contrast to nonrhizosphere soil, rhizosphere soil was dominated by rapidly growing microorganisms with the r strategy. The dependence of the dominant ecological strategy of the rhizosphere microbial community on the vegetation stage of plants has been traced. Study of the effect of plant species on the growth strategies of rhizosphere microorganisms showed that the features of the K strategy are more pronounced in the following rhizosphere microbial communities of grasses at the same growth stage: r strategy–Bromopsis inermis L.–Poa pratensis L., P. compressa L.–Dactylis glomerata L.–Festuca pratensisL.–K strategy. In the absence of limitation by climatic factors, the growth strategies of rhizosphere microorganisms are determined by the competition between microorganisms and plants for nutrients.     

贺兰山东麓荒漠藻结皮微生物群落结构及其演替研究

以宁夏贺兰山东麓荒漠藻结皮为研究对象,对处于不同发育阶段的藻结皮中微生物群落结构及其演替进行了研究。结皮样品高通量测序结果分别得到521个16S rDNA序列操作分类单元(OTU)和64个18S rDNA序列OTU,表明藻结皮中原核微生物多样性远高于真核微生物;贺兰山东麓藻结皮中原核微生物分布于26个纲,Cyanobacteria在各个发育阶段中都是优势微生物类群,Actinobacteria、Chloroplast、Alphaproteobacteria和Bacilli在藻结皮发育的各个阶段相对丰度也较高;从属水平上分析,Bacillus、Leptolyngbya、Microcoleus、Microvirga、Chroococcidiopsis、Rubellimicrobium、Phormidium、Mastigocladopsis、Skermanella、Nostoc、Scytonema共11个属在各个发育阶段的藻结皮中都存在,只是出现了丰度的差异。Bacillus在藻结皮形成期、发育初期和发育中期相对丰度较大,成熟期丰度显著下降,而成熟期Microvirga丰度较前3个时期显著增加,表现出明显的细菌菌群演替现象。藻结皮样品中主要真核微生物分布于13个纲,其中Dothideomycetes和Pezizomycetes在各个发育阶段样品中丰度都很高,Agaricomycetes在形成期样品中相对丰度高达32.6%,但在藻结皮发育过程中其相对丰度迅速下降;原生生物的相对丰度在藻结皮发育过程中逐渐增加;4个发育阶段藻结皮样品中均未检测到真核微藻序列。4个发育阶段的藻结皮样品中有明确分类学信息的真核微生物共13个属,其中4个发育阶段中共有的为Coniothyrium、Dendryphion、Friedmanniomyces、Phloeopeccania、Sarocladium共5个属,其余8个属只在个别发育阶段样品中检出,表明在藻结皮发育过程中真核微生物的群落结构也发生着变化。藻结皮厚度、全氮含量及有机质含量是影响结皮层微生物群落组成的主要因素。