Niche-directed evolution modulates genome architecture in freshwater Planctomycetes

Andrei, Adrian‐Ștefan; Salcher, Michaela M.; Mehrshad, Maliheh; Rychtecký, Pavel; Znachor, Petr; Ghai, Rohit

doi:10.1038/s41396-018-0332-5

Cited by 75 publications

(90 citation statements)

References 99 publications

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“…hypoxia, irregular nutrient input). Less obvious, but sporadic peaks are observed in the hypolimnion as well (Figure 3), what would suggest clonal expansions of the host, as has been reported for some Planctomycetes [59], suggesting similar dynamics are also played out in deeper waters.…”

Section: Resultssupporting

confidence: 57%

“…Eighteen water samples were collected from epilimnion (0.5m, n=10) and hypolimnion (30m, n=8) from June 2015 to August 2017. Two of these have been published previously [59,62] and the rest were generated in this study. Vertical profiles of the physicochemical characteristics of the water column (temperature, pH, oxygen; GRYF XBQ4, Havlíčkův Broc, CZ) and chlorophyll a (FluoroProbe TS-16-12, bbe Moldaenke, Kiel, Germany) were also taken.…”

Section: Methodsmentioning

confidence: 99%

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Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Kavagutti

Andrei

Mehrshad

et al. 2019

Preprint

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19The persistent inertia in the ability to culture environmentally abundant microbes from aquatic 20 ecosystems represents an obstacle in disentangling the complex web of ecological 21 interactions spun by a diverse assortment of participants (pro-and eukaryotes and their 22 viruses). In aquatic microbial communities, the numerically most abundant actors, the 23 viruses, remain the most elusive, and especially in freshwaters their identities and ecology 24 remain obscure. Here, using ultra-deep metagenomic sequencing from freshwater habitats Supplementary Table S1). While most samples we sequenced were ca. 54 Gb in size 87 (ranging from 190-482 million reads, average 368 million reads), two Římov samples (epi 88 and hypolimnion) we sequenced ca. 380 Gb each (2.5 billion reads each). An overview of the 89 microbial community using 16S rRNA abundances for both sites is shown in Supplementary 90 Figure S2. 91We also collected an additional 149 publicly available freshwater metagenomes 92 ( Supplementary Table S1, total of 4.04 billion reads, 1.09 Tb data) to search for complete 93 phage genomes. All datasets were assembled independently (no co-assembly). In total, we 94 analyzed ca. 3 Tb of metagenomic sequences from freshwater (ca. 17 billion reads). 95The number of complete phage genomes recovered from any sample increased with 96 sequencing depth, but with diminishing returns (Figure 1a), with genome recovery 97 maintaining linearity up to 100 Gb (ca. 1 phage genome for every additional Gb) before 98 tapering off at a maximum of 160 genomes from 400 Gb sequence data. While a total of 99 1677 genomes were assembled from the sequence data generated from the two study sites, 100(Římov and Jiřická), 357 genomes were recovered from all other available freshwater 101 metagenomes. This suggests that the potential of ultra-deep sequencing to recover far more 102 phage genomes has not yet been fully realized. We also recovered a number of 103 metagenome-assembled genomes (MAGs) from the Římov metagenome time-series dataset 104 (see below). We denominate this entire collection of genomes as the Uncultured Freshwater 105 Organisms (UFO) dataset, where the UFOv subset refers to viruses and the UFOp subset to 106 prokaryotic genomes. 107Phage genome analyses 108 A total of 598 complete phage genomes were recovered from the Římov epilimnion (10 109 samples), 800 from the hypolimnion (8 samples) and 279 from Jiřická (5 samples). Upon 110 dereplication (genomes with >95% identity and >95% coverage treated as one, see 111 methods), these numbers reduced by nearly three-fold for the hypolimnion suggesting 112 repeated capture of nearly identical genomes from multiple samplings. We found only a 113 single instance of a phage that was nearly identical in two habitats (Římov and Jiřická). 114The comparison of recovered freshwater phage genomes to representative sets of phages 115 from Viral RefSeq (1996 genomes) and the marine habitat (1335 genomes) [23-25] is shown 116 in Fig. 1c. Intriguingly, the genome size distributions of marin...

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Section: Resultssupporting

confidence: 57%

Section: Methodsmentioning

confidence: 99%

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Kavagutti

Andrei

Mehrshad

et al. 2019

Preprint

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“…The sample from the aphotic hypolimnion of Lake Zurich (aerobic but only 80 m deep) was used as a freshwater reference due to the scarcity of available metagenomes from deeper lakes. In addition, Lake Zurich has been extensively studied by both classical and metagenomic tools (Salcher et al 2015;Neuenschwander et al 2017;Mehrshad et al 2018b;Andrei et al 2019). As shown in Fig.…”

Section: Overall Similarity To Other Aphotic Freshwater and Marine Mementioning

confidence: 99%

Microbiome of the deep Lake Baikal, a unique oxic bathypelagic habitat

Cabello‐Yeves

Zemskaya

Zakharenko

et al. 2019

Limnology & Oceanography

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Lake Baikal is the deepest lake in the world. Its depth provides the only bathypelagic (> 1000 m deep) freshwater habitat on Earth and its oxic, ultra-oligotrophic features make it a freshwater counterpart of the deep ocean. Here we have analyzed metagenomes from 1250 and 1350 m deep samples and built 231 metagenome-assembled genomes (MAGs). We detected high fractions of Thaumarchaeota (ca. 20% of 16S rRNA reads) and members of the candidate phyla radiation (CPR) (3-4.5%). Among the MAGs, we obtained ammonia-oxidizing archaea (AOA, Nitrosopumilaceae) and bacteria (AOB, Nitrosomonadaceae), and nitrite-oxidizers (Nitrospirae) indicating very active nitrification. A new clade of freshwater SAR202 Chloroflexi and methanotrophs (Methyloglobulus) were also remarkably abundant, the latter reflecting a possible role of methane oxidation as well. Novel species of streamlined and cosmopolitan bacteria such as Ca. Fonsibacter or acI Actinobacteria were more abundant at the surface but also present in deep waters. Conversely, CPRs, Myxococcales, Chloroflexi, DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota) archaea, or Gammaproteobacteria were found only in bathypelagic samples. We noted various important taxonomic and metabolic differences between deep aphotic region of Lake Baikal and marine waters of similar depth: Betaproteobacteriales, CPR, and DPANN superphylum were only found in bathypelagic Baikal, while Deltaproteobacteria, Gammaproteobacteria, or Alphaproteobacteria prevailed in oceanic samples. The genes mediating ammonia and methane oxidation, aromatic compound degradation, or alkane/methanesulfonate monooxygenases were detected in higher numbers in deep Baikal compared to their oceanic counterparts or its own surface. Overall, depth seems to be less relevant than salinity in configuring the microbial community.

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“…Although the genome size differed by more than fivefold, core genome metabolism, such as "E Amino acid transport and metabolism," "G Carbohydrate transport and metabolism," and "H Coenzyme transport and metabolism" remained constant. If genome streamlining represents an adaptive evolution from sediment/soil transition to aquatic environments (Andrei et al 2019), the relative large genomes may indicate massive gene equipment in environments where resources are scarce but diverse and where there is little penalty for slow growth (Konstantinidis and Tiedje 2005), such as the hypolimnion of deep lakes.…”

Section: Discussionmentioning

confidence: 99%

“…The evolutionary relationships and the taxonomic ranks of the 84 Planctomycetes MAGs were investigated through phylogenomic analysis (Supporting Information Table S5). A maximum likelihood tree (360 Planctomycetes-specific genes) was constructed based on all of the single genomes and metagenomics-recovered representatives published by Andrei et al (2019) (Fig. 6).…”

Section: Planctomycetes Diversity and Candidatus New Classmentioning

confidence: 99%

Stratification of microbiomes during the holomictic period of Lake Fuxian, an alpine monomictic lake

Xing

Tao

Luo

et al. 2019

Limnology & Oceanography

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In warm monomictic lakes, the hypolimnion is important for accumulating and decomposing organic matter derived from surface production, and the regenerated nutrients will be supplied to the epilimnion through winter vertical mixing. So far, we know little about microbial community composition and function in the hypolimnion when the significant thermal stratification disappears. In this study, we investigated microbial community compositions and functional gene contents by means of metagenomics along a depth profile in the warm monomictic alpine Lake Fuxian during holomictic period. Overall, bacteria were the dominant microbial group at different water depths, while phages had their high relative abundance in the epilimnion. We observed slight thermal but strong chemical stratification even during this typical winter overturn. The anaerobic respiration with nitrate and sulfate as the terminal electron acceptors was accumulated at bottom of hypolimnionin as indicated through metabolic pathway reconstruction. We were able to get 440 metagenome-assembled genomes (MAGs) and unraveled a high genomic diversity of freshwater pelagic microbiomes along this depth profile. We furthermore defined a new class of "Plancto_FXH1" of Planctomycetes from these MAGs, of which a distinct nitrate reduction operon was identified. Representatives of this phylum mainly thrive in the hypolimnion as previously suspected, but few lineages were detected in the epilimnion. In summary, metagenomics enabled us to find a new group of Planctomycetes, probably involved in denitrification in the hypolimnion in Lake Fuxian, which expand our knowledge on denitrifying bacterial diversity and their denitrification potential in deep freshwater lakes.

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Niche-directed evolution modulates genome architecture in freshwater Planctomycetes

Cited by 75 publications

References 99 publications

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Microbiome of the deep Lake Baikal, a unique oxic bathypelagic habitat

Stratification of microbiomes during the holomictic period of Lake Fuxian, an alpine monomictic lake

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