Dynamic cellular complexity of anoxygenic phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno

Danza, Francesco; Storelli, Nicola; Roman, Samuele; Luedin, Samuel M.; Tonolla, Mauro

doi:10.1371/journal.pone.0189510

Cited by 24 publications

(46 citation statements)

References 56 publications

(82 reference statements)

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“…To complete the photosynthetic water column analysis and to evidence possible microbial interactions between different lake compartments, FCM was applied as a rapid tool to detect photosynthetic microorganisms signature, as demonstrated in earlier studies [27,36,37]. Our FCM analyses of phototrophic microbial populations revealed unexpected yearly dynamics in community composition with possible effects on water column stability (Fig 5).…”

Section: Discussionmentioning

confidence: 63%

“…It has been suggested that reduced incident light towards the end of the vegetative period favor the growth of large-celled PSB over that of small-celled PSB [55]. However, that study and a companion study [27] suggest that microbial community dynamics in Lake Cadagno might be strongly influenced by intra- and interspecific interactions.…”

Section: Discussionmentioning

confidence: 97%

“…For the detection of autofluorescent phototrophic bacteria in the water column, FCM was used to determine chlorophyll/bacteriochlorophyll and phycobilin signatures as described in previous studies [27,36,37]. We used a BD Accuri C6 cytometer (Becton Dickinson, San José, CA, USA) device equipped with two lasers (488 nm, 680 nm), two scatter detectors, and four fluorescence detectors (laser 488nm: FL1 = 533/30, FL2 = 585/40, FL3 = 670; laser 640 nm: FL4 = 670).…”

Section: Methodsmentioning

confidence: 99%

“…Sample analysis was limited to 50 μL with fluidic flow rate of 66 μL min -1 and samples were diluted if necessary in order to achieve a maximum of 1’000 events per mL. Green sulfur (GSB) and purple sulfur bacteria (PSB) colonizing the chemocline of Lake Cadagno were distinguished through FCM based on morphological characters as described by Danza et al [27]. Among PSB, large-celled C .…”

Section: Methodsmentioning

confidence: 99%

“…The coexistence of phylogenetically distinct bacteria with substantial metabolic redundancy such as PSB and GSB might be relevant for maintenance of key ecosystem functions in Lake Cadagno. However, yet unknown differences in other functional characteristics of the species involved are required to explain their coexistence [27]. Although anoxygenic phototrophic sulfur bacteria are confined to the chemocline, they interact with the bacterial community in adjacent strata of the water column [18].…”

Section: Introductionmentioning

confidence: 99%

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Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics

et al. 2018

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The meromictic Lake Cadagno is characterized by a compact chemocline with high concentrations of anoxygenic phototrophic purple and green sulfur bacteria. However, a complete picture of the bacterial diversity, and in particular of effects of seasonality and compartmentalization is missing. To characterize bacterial communities and elucidate relationships between them and their surrounding environment high-throughput 16S rRNA gene pyrosequencing was conducted. Proteobacteria, Chlorobi, Verrucomicrobia, and Actinobacteria were the dominant groups in Lake Cadagno water column. Moreover, bacterial interaction within the chemocline and between oxic and anoxic lake compartments were investigated through fluorescence in situ hybridization (FISH) and flow cytometry (FCM). The different populations of purple sulfur bacteria (PSB) and green sulfur bacteria (GSB) in the chemocline indicate seasonal dynamics of phototrophic sulfur bacteria composition. Interestingly, an exceptional bloom of a cyanobacteria population in the oxic-anoxic transition zone affected the common spatial distribution of phototrophic sulfur bacteria with consequence on chemocline location and water column stability. Our study suggests that both bacterial interactions between different lake compartments and within the chemocline can be a dynamic process influencing the stratification structure of Lake Cadagno water column.

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Section: Discussionmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics

et al. 2018

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Persistence of bioconvection‐induced mixed layers in a stratified lake

Steiner

Bouffard

Wüest

2021

Limnology & Oceanography

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In situ observations of biophysical interactions in natural waters typically focus on physical mechanisms influencing biological activity. Yet, biological activity can also drive physical processes in aquatic environments. A community of photoautotrophic, motile and heavy bacteria—Chromatium okenii, which requires light, sulfide, and anoxic conditions to perform anoxygenic photosynthesis, accumulates below the chemocline of the meromictic Lake Cadagno (Switzerland). Upward vertical migration drives bioconvection, which modifies the physical environment of the bacteria‐populated water to create a deep and homogeneous mixed layer of up to 1 m thickness. Continuous convection within the mixed layer and diapycnal diffusivity from its adjacent stratified surroundings determine ecologically relevant gradients. The daytime vertical migration that induce convective instabilities is well‐established. It consists in bacteria swimming upward towards light and accumulating at the upper part of the anoxic layer, leading to a locally‐unstable density excess. However, nocturnal activity has not yet been analyzed. An intensive 48‐h survey was conducted in August 2018 using standard and microstructure profilers, as well as a moored high‐resolution current meter coupled with temperature and turbidity sensors deployed across the mixed layer depth. This survey revealed a persistent mixed layer also during nighttime hours. Using a mixed layer shape model, vertical velocity observations and turbulent dissipation estimates, we conclude that photoautotrophic bacteria continue their vertical migration at night. This nocturnal activity thereby drives “dark bioconvection” and maintains the subsurface mixed bacterial layer in Lake Cadagno throughout the diel cycle.

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Vertical niche occupation and potential metabolic interplay of microbial consortia in a deeply stratified meromictic model lake

Cabello‐Yeves,

Picazo,

Roda‐Garcia

et al. 2023

Limnology & Oceanography

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The microbial ecology of meromictic lakes assessed with “omics” is still poorly studied compared to other aquatic systems. Here, a combination of metagenomics, high resolution sampling and detailed physical–chemical data gathering allowed to study the planktonic prokaryotic assemblages and metabolic capabilities in the crenogenic meromictic Lake El Tobar (Spain), a model lake for such purposes. This system presents a specific stratification comprising a freshwater layer and a halocline linked to the oxycline, driving to the euxinic hypersaline waters of the deep monimolimnion. The different strata showed a highly diverse and vertically distributed microbiome with their metabolic capacities fitting/influencing the physical–chemical environment. Overall, up to 338 novel genomes were found from metagenome assembled genomes. Picocyanobacteria and methanotrophs were abundant in the upper part of the oxycline. Anoxygenic phototrophs (Chlorobium, Thiohalocapsa, Chromatiaceae, Rhodospirillum, and Rhodobacteraceae spp.) dominated the 12.5–14 m anoxic waters with dim light availability. Sulfate reducers (Desulfobacterota and Firmicutes) inhabited low redox horizons from 13.5 to the bottom (18 m). The potential microbial synergistic performance increases toward the monimolimnion. Among these, a microbial assemblage mostly composed of Spirochaetota, Cloacimonadota, Omitrophota, Firmicutes, Marinisomatota, Nanoarchaeota, and Patescibacteria in hypersaline waters of 14–18 m (conductivities of 118–213 mS cm−1), is potentially capable of performing mixed‐acid fermentations, even including hydrogen and butanol biosynthesis of biotechnological interest. This metagenomics study shows how microbial lifestyles may be determinant in the interplay of environmental gradients, and exemplifies the potential interactions between the microbial guilds thereby.

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Dynamic cellular complexity of anoxygenic phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno

Cited by 24 publications

References 56 publications

Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics

Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics

Persistence of bioconvection‐induced mixed layers in a stratified lake

Vertical niche occupation and potential metabolic interplay of microbial consortia in a deeply stratified meromictic model lake

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