A Guide to the Natural History of Freshwater Lake Bacteria

Summary: Freshwater bacteria are at the hub of biogeochemical cycles and control water quality in lakes. Despite this, little is known about the identity and ecology of functionally significant lake bacteria. Molecular studies have identified many abundant lake bacteria, but there is a large variation in the taxonomic or phylogenetic breadths among the methods used for this exploration. Because of this, an inconsistent and overlapping naming structure has developed for freshwater bacteria, creating a significant obstacle to identifying coherent ecological traits among these groups. A discourse that unites the field is sorely needed. Here we present a new freshwater lake phylogeny constructed from all published 16S rRNA gene sequences from lake epilimnia and propose a unifying vocabulary to discuss freshwater taxa. With this new vocabulary in place, we review the current information on the ecology, ecophysiology, and distribution of lake bacteria and highlight newly identified phylotypes. In the second part of our review, we conduct meta-analyses on the compiled data, identifying distribution patterns for bacterial phylotypes among biomes and across environmental gradients in lakes. We conclude by emphasizing the role that this review can play in providing a coherent framework for future studies.     

富营养化城市湖泊武汉东湖沉积物微生物群体结构及空间变化研究(英文)北大核心CSCD

【目的】城市湖泊沉积物中的微生物群体是富营养环境生物修复的重要因素。本研究拟对中型富营养化湖泊——武汉东湖沉积物细菌群体结构及空间变化规律进行研究。加深对富营养湖泊微生物群体结构的理解,并为城市湖泊的保护和污染控制提供参考。【方法】采用16S r RNA基因RFLP分析和序列分析技术获得细菌群体系统发育信息。采用PCoA法分析武汉东湖沉积物细菌群体内以及与其它湖泊沉积物细菌群体间的相似性。采用CCA法分析环境因素对细菌群体的影响。【结果】武汉东湖沉积物细菌群体包含13个门和2个未知种群。PCoA分析进一步表明来自东湖3个子湖的细菌群体与其它地域富营养化湖泊的微生物种群结构相似,并区别于重度富营养化子湖庙湖的细菌群体。在庙湖中,我们发现了Thermogymnomonas类古菌的含量显著偏高。CCA分析表明细菌的分布与沉积物中碳、氮和磷元素的含量显著相关。【结论】本研究进一步确证了环境因素对细菌群体组成和分布的调节作用,加深了对富营养水体微生物群体结构的理解,并为城市湖泊的保护和污染控制提供了参考。     

Abundance and diversity of aerobic anoxygenic phototrophic bacteria in saline lakes on the Tibetan plateau

Aerobic anoxygenic phototrophic (AAP) bacteria are heterotrophic prokaryotes that are capable of utilizing light as an energy source but are not capable of producing molecular oxygen. Recently, multiple studies have found that AAP bacteria are widely distributed in oceans and estuaries and may play an important role in carbon cycling. However, AAP bacteria in inland lake ecosystems have not been investigated in depth. In this study, the abundance and diversity of the pufL-M genes, encoding photosynthetic reaction centers of AAP bacteria, were determined in the oxic water column and anoxic sediments of saline lakes (Qinghai, Erhai, and Gahai Lakes) on the Tibetan Plateau, China. Our results indicated that AAP bacteria were abundant in inland lakes, with the proportion of AAP bacteria (in total bacteria) comparable to those in the oceans, but with a lower diversity. Salinity and pH were found to be potential factors controlling the AAP bacterial diversity and community composition. Our data have implications for a better understanding of the potential role of AAP bacteria in carbon cycling in inland lake ecosystems.     

Diversity of sulfur-cycle prokaryotes in freshwater lake sediments investigated using aprA as the functional marker gene

The diversity of sulfate-reducing prokaryotes (SRPs) and sulfur-oxidizing prokaryotes (SOPs) in freshwater lake ecosystems was investigated by cloning and sequencing of the aprA gene, which encodes for a key enzyme in dissimilatory sulfate reduction and sulfur oxidation. To understand their diversity better, the spatial distribution of aprA genes was investigated in sediments collected from six geographically distant lakes in Antarctica and Japan, including a hypersaline lake for comparison. The microbial community compositions of freshwater sediments and a hypersaline sediment showed notable differences. The clones affiliated with Desulfobacteraceae and Desulfobulbaceae were frequently detected in all freshwater lake sediments. The SOP community was mainly composed of four major phylogenetic groups. One of them formed a monophyletic cluster with a sulfur-oxidizing betaproteobacterium, Sulfuricella denitrificans, but the others were not assigned to specific genera. In addition, the AprA sequences, which were not clearly affiliated to either SRP or SOP lineages, dominated the libraries from four freshwater lake sediments. The results showed the wide distribution of some sulfur-cycle prokaryotes across geographical distances and supported the idea that metabolic flexibility is an important feature for SRP survival in low-sulfate environments.     

Viable endospores of Thermoactinomyces vulgaris in lake sediments as indicators of agricultural history

Bacteria of the genus Thermoactinomyces form endospores with an extreme longevity in natural habitats. We isolated Thermoactinomyces sacchari from 9,000-year-old varved (annually laminated) sediment; thus, T. sacchari is probably one of the oldest known living organisms. More importantly, we tested and verified the hypothesis that there is a relationship between concentrations of dormant, viable endospores of T. vulgaris in lake sediments and the extent of agriculture in the catchments of the lakes. In surface sediments, low concentrations were recorded in forest lakes and the concentrations increased with increasing areas of cultivated land around the lakes. In varved sediment cores from three lakes, we found a temporal relationship between records of T. vulgaris endospores and the pollen of plants indicating agriculture. Endospores were very rare in sediments deposited before agriculture, ca. 1100 A.D. From then to between 1300 and 1700 A.D., a period with restricted cultivation, low but more regular rates of accumulation of endospores were recorded. High endospore accumulation rates were found with the subsequent agricultural expansion. This investigation confirms suggestions that this bacterium could be used as a paleoindicator for agricultural activity and be complementary to pollen analyses. Viable bacteria in continuous records of lake sediments are also potential material for evolutionary studies.     

Viable endospores of Thermoactinomyces vulgaris in lake sediments as indicators of agricultural history.

Bacteria of the genus Thermoactinomyces form endospores with an extreme longevity in natural habitats. We isolated Thermoactinomyces sacchari from 9,000-year-old varved (annually laminated) sediment; thus, T. sacchari is probably one of the oldest known living organisms. More importantly, we tested and verified the hypothesis that there is a relationship between concentrations of dormant, viable endospores of T. vulgaris in lake sediments and the extent of agriculture in the catchments of the lakes. In surface sediments, low concentrations were recorded in forest lakes and the concentrations increased with increasing areas of cultivated land around the lakes. In varved sediment cores from three lakes, we found a temporal relationship between records of T. vulgaris endospores and the pollen of plants indicating agriculture. Endospores were very rare in sediments deposited before agriculture, ca. 1100 A.D. From then to between 1300 and 1700 A.D., a period with restricted cultivation, low but more regular rates of accumulation of endospores were recorded. High endospore accumulation rates were found with the subsequent agricultural expansion. This investigation confirms suggestions that this bacterium could be used as a paleoindicator for agricultural activity and be complementary to pollen analyses. Viable bacteria in continuous records of lake sediments are also potential material for evolutionary studies.     

Functional Groups and Activities of Bacteria in a Highly Acidic Volcanic Mountain Stream and Lake in Patagonia,Argentina

Acidic volcanic waters are naturally occurring extreme habitats that are subject of worldwide geochemical research but have been little investigated with respect to their biology. To fill this gap, the microbial ecology of a volcanic acidic river (pH approximately equal to 0-1.6), Rio Agrio, and the recipient lake Caviahue in Patagonia, Argentina, was studied. Water and sediment samples were investigated for Fe(II), Fe(III), methane, bacterial abundances, biomass, and activities (oxygen consumption, iron oxidation and reduction). The extremely acidic river showed a strong gradient of microbial life with increasing values downstream and few signs of life near the source. Only sulfide-oxidizing and fermentative bacteria could be cultured from the upper part of Rio Agrio. However, in the lower part of the system, microbial biomass and oxygen penetration and consumption in the sediment were comparable to non-extreme aquatic habitats. To characterize similarities and differences of chemically similar natural and man-made acidic waters, our findings were compared to those from acidic mining lakes in Germany. In the lower part of the river and the lake, numbers of iron and sulfur bacteria and total biomass in sediments were comparable to those known from acidic mining lakes. Bacterial abundance in water samples was also very similar for both types of acidic water (around 10(5) mL(-1)). In contrast, Fe(II) oxidation and Fe(III) reduction potentials appeared to be lower despite higher biogenic oxygen consumption and higher photosynthetic activity at the sediment-water interface. Surprisingly, methanogenesis was detected in the presence of high sulfate concentrations in the profundal sediment of Lake Caviahue. In addition to supplementing microbiological knowledge on acidic volcanic waters, our study provides a new view of these extreme sites in the general context of aquatic habitats.     

Molecular Detection of Novel Anammox Bacterial Clusters in the Sediments of the Shallow Freshwater Lake Taihu

Previous studies have demonstrated the wide occurrence of anaerobic ammonium oxidizing (anammox) bacteria; however, there is very limited information on the distribution of these bacteria in freshwater habitats. In this study, the anammox bacterial communities were detected by molecular analysis targeting the 16S rRNA genes in the sediments of Lake Taihu, a large and shallow eutrophic freshwater lake in China. The recovery of specific 16S rRNA sequences with two stable monophyletic clusters indicated that anammox bacteria were present in Lake Taihu. A phylogenetic analysis indicated that these two groups represent two novel lineages within the first subgroup of anammox bacteria, independent of the treeing methods. High intra-lake variability in anammox bacterial diversity and community composition was observed, in particular, based on a 1% cut-off of 16S rRNA sequence variation. The spatial variability was largely related to the substrate availability, which was denoted by the correlations between the relative abundance of the two Taihu anammox bacterial groups and the concentrations of ammonium and nitrite. This indicates that the niche differentiation of anammox bacteria is linked to the environmental heterogeneity. These findings suggest that the freshwater lakes may accommodate different anammox bacterial communities and, thus, expand our knowledge on the diversity and distribution of anammox bacteria. Supplemental materials are available for this article. Go to the publisher's online edition of Geomicrobiology Journal to view the free supplemental files.     

Dynamics of Nitrification and Denitrification in Root-Oxygenated Sediments and Adaptation of Ammonia-Oxidizing Bacteria to Low-Oxygen or Anoxic Habitats

Oxygen-releasing plants may provide aerobic niches in anoxic sediments and soils for ammonia-oxidizing bacteria. The oxygen-releasing, aerenchymatous emergent macrophyte Glyceria maxima had a strong positive effect on numbers and activities of the nitrifying bacteria in its root zone in spring and early summer. The stimulation of the aerobic nitrifying bacteria in the freshwater sediment, ascribed to oxygen release by the roots of G. maxima, disappeared in late summer. Numbers and activities of the nitrifying bacteria were positively correlated, and a positive relationship with denitrification activities also was found. To assess possible adaptations of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats, a comparison was made between the freshwater lake sediment and three soils differing in oxicity profiles. Oxygen kinetics and tolerance to anoxia of the ammonia-oxidizing communities from these habitats were determined. The apparent K(infm) values for oxygen of the ammonia-oxidizing community in the lake sediment were in the range of 5 to 15 (mu)M, which was substantially lower than the range of K(infm) values for oxygen of the ammonia-oxidizing community from a permanently oxic dune location. Upon anoxic incubation, the ammonia-oxidizing communities of dune, chalk grassland, and calcareous grassland soils lost 99, 95, and 92% of their initial nitrifying capacity, respectively. In contrast, the ammonia-oxidizing community in the lake sediment started to nitrify within 1 h upon exposure to oxygen at the level of the initial capacity. It is argued that the conservation of the nitrifying capacity during anoxic periods and the ability to react instantaneously to the presence of oxygen are important traits of nitrifiers in fluctuating oxic-anoxic environments such as the root zone of aerenchymatous plant species.     

Multifaceted aspects of synchrony between freshwater prokaryotes and protists

Community composition of freshwater prokaryotes and protists varies through time. Few studies contemporarily investigate temporal variation of these freshwater communities for more than 1 year. We compared the temporal patterns of prokaryotes and protists in three distinct habitats for 4 years (2014–2017) in Lake Tovel, a cold‐water lake. This lake showed a marked temperature increase in 2017 linked to altered precipitation patterns. We investigated whether microbial communities reflected this change across habitats and whether changes occurred at the same time and to the same extent. Furthermore, we tested the concept of hydrological year emphasizing the ecological effect of water renewal on communities for its explanatory power of community changes. Microbe diversity was assessed by Illumina sequencing of the V3–V4 hypervariable region of the 16S rRNA gene and 18S rRNA gene, and we applied co‐inertia analysis and asymmetric eigenvector maps modelling to infer synchrony and temporal patterns of prokaryotes and protists. When considering community composition, microbes were invariable in synchrony across habitats and indicated a temporal gradient linked to decreasing precipitation; however, when looking at temporal patterns, the extent of synchrony was reduced. Small‐scale patterns were similar across habitats and microbes and linked to seasonally varying environmental variables, while large‐scale patterns were different and partially linked to an ecosystem change as indicated by increasing water transparency and temperature and decreasing dissolved oxygen. Our advanced statistical approach outlined the multifaceted aspect of synchrony when linked to community composition and temporal patterns.     

The effects of submerged aquatic vegetation on the persistence of environmental populations of Enterococcus spp.

Enterococcus spp. are utilized worldwide as faecal indicator bacteria, but certain strains exhibit extended survival in environmental habitats and the factors influencing their persistence are poorly understood. We used flowing freshwater mesocosms to explore the effect of submerged aquatic vegetation (SAV) on the persistence of natural enterococci populations from a subtropical lake. The highest mean densities of culturable enterococci over 2 weeks occurred in SAV [8.6 × 10² colony‐forming units (cfu) per 100 g wet weight], followed by sediments (1.3 × 10² cfu per 100 g) and water (18 cfu per 100 ml). However, due to relative differences in the total mass of each substrate in the entire system (water > sediments > SAV), SAV‐associated enterococci represented only a minor proportion of the total population. Vegetated mesocosms harboured significantly higher mean cfu per mesocosm and cfu densities in sediments compared with their unvegetated counterparts, suggesting that SAV indirectly facilitates persistence in aquatic habitats. Populations were dominated (> 96%) by a single Enterococcus casseliflavus strain according to BOX‐PCR genotyping, which did not change over the 10‐month study and strongly suggests bacterial replication in the lake. The presence of such strains in the environment may represent highly competitive, naturalized and reproducing indicator bacteria populations that are not directly related to pollution events.     

Development of a real-time PCR method for the detection of fossil 16S rDNA fragments of phototrophic sulfur bacteria in the sediments of Lake Cadagno

Lake Cadagno is a crenogenic meromictic lake situated in the southern range of the Swiss Alps characterized by a compact chemocline that has been the object of many ecological studies. The population dynamics of phototrophic sulfur bacteria in the chemocline has been monitored since 1994 with molecular methods such as 16S rRNA gene clone library analysis. To reconstruct paleo-microbial community dynamics, we developed a quantitative real-time PCR methodology for specific detection of 16S rRNA gene sequences of purple and green sulfur bacteria populations from sediment samples. We detected fossil 16S rDNA of nine populations of phototrophic sulfur bacteria down to 9-m sediment depth, corresponding to about 9500 years of the lake's biogeological history. These results provide the first evidence for the presence of 16S rDNA of anoxygenic phototrophic bacteria in Holocene sediments of an alpine meromictic lake and indicate that the water column stratification and the bacterial plume were already present in Lake Cadagno thousands of years ago. The finding of Chlorobium clathratiforme remains in all the samples analyzed shows that this population, identified in the water column only in 2001, was already a part of the lake's biota in the past.     

Phylogenetic systematics of microorganisms inhabiting thermal environments

Thermal habitats harbor specialized communities of thermophilic microorganisms, primarily prokaryotes. This review considers modern systematics of prokaryotes and the place of thermophilic archaea and bacteria in it. Among the existing hierarchical classifications of prokaryotes, the bulk of attention is given to the one accepted in the current second edition of "Bergey's Manual of Systematic Bacteriology", which is primarily based on 16S rRNA phylogeny and phenotypic properties of the organisms. Analysis of the genomics data shows that they on the whole agree with the 16S rRNA-based system, although revealing the significance of the evolutionary role of lateral transfer, duplication, and loss of genes. According to the classification elaborated in the current edition of "Bergey's Manual", the prokaryotes currently culturable under laboratory conditions are distributed among 26 phyla, two of which belong to the domain Archaea and 24 to the domain Bacteria. Six phyla contain exclusively thermophiles, and eleven phyla contain thermophiles along with mesophiles, thermophiles being usually separated phylogenetically and representing high-level taxa (classes, orders). In light of the data on the topology of the 16S rRNA-based phylogenetic tree and some other data, this review discusses the probable hyperthermophilic nature of the universal common ancestor.     

Large differences in the fraction of active bacteria in plankton,sediments, and biofilm

Generally, only a small fraction of free-living pelagic bacteria are metabolically active, while particle-associated bacteria usually exhibit a larger proportion of active bacteria. Most previous studies on the active fraction of bacteria focus on planktonic communities, and there are only a few studies on sediment and epiphytic biofilm bacteria. We compared the active fraction of the total number of bacteria in three different habitats of the littoral zone of Lake Erken, Sweden, including the sediments, the epiphytic biofilm on the submerged macrophyte Ranunculus circinatus, and the water column. Active bacteria were detected as those with an active electron transport system, identified by the capacity to reduce the tetrazolium salt CTC (5-cyano-2,3-ditolyltetrazolium chloride) into its fluorescent, water insoluble state. There were large differences between habitats. The active fraction of the total number of bacteria detected by fluorescence microscopy (annual mean +/- SD) in the sediments was 46 +/- 10%, on R. circinatus 37 +/- 18%, and in the water column 4 +/- 4%. The abundance of CTC-reducing cells was correlated with total bacterial abundance, and the fraction of CTC-reducing bacteria generally increased with total bacterial abundance, for all the habitats. Consequently, the difference in the fraction of CTC-reducing bacteria between the habitats could be attributed to different densities of bacteria, with a larger proportion of active bacteria at higher bacterial densities.     

Microbial horizontal gene transfer and the DNA release from transgenic crop plants

Intraspecific and interspecific horizontal gene transfers among prokaryotes by mechanisms like conjugation, transduction and transformation are part of their life style. Experimental data and nucleotide sequence analyses show that these processes appear to occur in any prokaryotic habitat and have shaped microbial genomes throughout evolution over hundreds of million years. Here we summarize studies with a focus on the possibility of the transfer of free recombinant DNA released from transgenic plants to microorganisms by transformation. A list of 87 species capable of natural transformation is presented. We discuss monitoring techniques which allowed detection of the spread of intact DNA from plants during their growth, in the process of decay and by pollen dispersal including novel biomonitoring assays for measuring the transforming potential of DNA in the environment. Also, studies on the persistence of free DNA in soil habitats and the potential of bacteria to take up DNA in soil are summarized. On the other hand, the various barriers evolved in prokaryotes which suppress interspecific gene transfer and recombination will be addressed along with studies aiming to estimate the chance of a gene transfer from plant to microbe. The results suggest that, although such transfers could be possible in principle, each of the many steps involved from the release of intact DNA from a plant cell to integration into a prokaryotic genome has such a low probability that a successful transfer event be extremely rare. Further, interspecies transfer of chromosomal DNA is mostly negative for the recipient, and, if not, in the absence of a selective advantage the transformant will be lost. It is stressed that the nucleotide sequences introduced into transgenic plants are much less likely to be captured from the transgenic plants than directly from those organisms (often bacteria or viruses) from which they were originally derived.     

A review of dystrophic lake and pool habitat in Europe: An Irish perspective

Freshwater lakes and pools contained within peatlands are unique habitats that support rare and specialised species. Despite this, these ecosystems have been overlooked in conservation and management practices. One of these habitats, ‘3160 Natural dystrophic lakes and ponds’, is protected under the European Union (EU) Habitats Directive with a concerning proportion of these habitats having an “unfavourable-bad” or an “unfavourable-inadequate” conservation status across Europe. Our current understanding of the key physico-chemical and ecological features of this habitat is inadequate which is hindering the implementation of effective conservation measures. This review summarises the current knowledge of this protected lake habitat as defined under the EU Habitats Directive. With a focus on Ireland, we demonstrate how the current monitoring and assessment methods used to characterise and assess the structure and function and conservation status of this habitat, which relies largely on the use of macrophyte community composition and surrogate physico-chemical data collected under the EU Water Framework Directive, is ineffective. We propose the incorporation of further or alternative ecological metrics including, but not limited to, algae and macroinvertebrates which are needed to improve our understanding of the structure and function of this priority lake habitat. In addition, application of such data via ecological metrics would allow for the quantification of biodiversity and species rarity metrics which would aid in identifying sites of conservation importance.     

Structure and activity of lacustrine sediment bacteria involved in nutrient and iron cycles

Knowledge of the bacterial community structure in sediments is essential to better design restoration strategies for eutrophied lakes. In this regard, the aim of this study was to quantify the abundance and activity of bacteria involved in nutrient and iron cycling in sediments from four Azorean lakes with distinct trophic states (Verde, Azul, Furnas and Fogo). Inferred from quantitative PCR, bacteria performing anaerobic ammonia oxidation were the most abundant in the eutrophic lakes Verde, Azul and Furnas (4.5-16.6%), followed by nitrifying bacteria (0.8-13.0%), denitrifying bacteria (DNB) (0.5-6.8%), iron-reducing bacteria (0.2-1.4%) and phosphorus-accumulating organisms (<0.3%). In contrast, DNB dominated sediments from the oligo-mesotrophic lake Fogo (8.8%). Activity assays suggested that bacteria performing ammonia oxidation (aerobic and anaerobic), nitrite oxidation, heterothrophic nitrate reduction, iron reduction and biological phosphorus storage/release were present and active in all Azorean lake sediments. The present work also suggested that the activity of DNB might contribute to the release of phosphorus from sediments.     

环境DNA在湖泊生物多样性研究中的应用

环境DNA(EnvironmentalDNA,eDNA)可用于监测湖泊生物多样性,该技术对湖泊生态环境破坏性小,对于开展湖泊生态保护具有重要意义.湖泊流速较为缓慢,相对于河流更容易富集DNA,更适合于应用eDNA方法开展生物多样性研究.文章对eDNA在湖泊生物多样性上的应用进行了回顾,综述了其实验设计,分析了该技术存在...     

Virus-host interactions in salt lakes

Natural hypersaline waters are widely distributed around the globe, as both continental surface waters and sea floor lakes, the latter being maintained by the large density difference between the hypersaline and overlying marine water. Owing to the extreme salt concentrations, close to or at saturation (approximately 35%, w/v), such waters might be expected to be devoid of life but, in fact, maintain dense populations of microbes. The majority of these microorganisms are halophilic prokaryotes belonging to the Domain Archaea, 'haloarchaea'. Viruses infecting haloarchaea are a vital part of hypersaline ecosystems, in many circumstances outnumbering cells by 10-100-fold. However, few of these 'haloviruses' have been isolated and even fewer have been characterised in molecular detail. In this review, we explore the methods used by haloviruses to replicate within their hosts and consider the implications of haloviral-haloarchaeal interactions for salt lake ecology.     

A comparison of 35S-SO(4)(2-) radiotracer techniques to determine sulphate reduction rates in laminated sediments

In order to find a simple and efficient method to determine sulphate reduction rates in environmental samples, we tested different 35S-SO(4)(2-) radiotracer techniques. The methods varied in the application of 35S-SO(4)(2-) and subsequent extraction of reduced 35S-sulphur species. Samples were either incubated as sediment slurries mixed with the radiotracer, or as undisturbed sediment cores after core injection of the radiotracer. Reduced 35S-sulphur species were retrieved passively by diffusion or actively by reflux distillation. The methods were applied to surface sediments derived from three aquatic habitats situated in Germany: (1) a tideless brackish water, (2) a mining lake and (3) a natural freshwater lake. The best possible method was expected to yield the highest sulphate reduction rates, which were reproducible with respect to magnitude and depth distribution. At the same time, we aimed to keep the disturbance of samples as well as the expenditure of labour and equipment to a minimum. For all three types of aquatic habitats, the combination of core injection followed by diffusion was the most reliable and efficient method. This combination is therefore recommended for determination of sulphate reduction rates in laminated sediments.