Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria

Fecskeová, Lívia Kolesár; Piwosz, Kasia; Hanusová, Martina; Nedoma, Jiří; Znachor, Petr; Koblížek, Michal

doi:10.1038/s41598-019-55210-x

Cited by 22 publications

(28 citation statements)

References 68 publications

(90 reference statements)

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“…In support of the true photoheterotrophic nature of Gemmatimonadota, a previous study conducted in Rímov Reservoir, found active expression of their pufM genes (a common molecular marker gene for aerobic anoxygenic phototrophs) (27). Expression of the photosynthetic apparatus of Gemmatimonadota showed that they are an active part of bacterial community and do not just passively contain the phototrophic genes (27).…”

Section: Discussionmentioning

confidence: 90%

“…It has been suggested that Gemmatimonadota may be relatively more abundant in dry soils ( 26 ). On the other hand, from the available data, it is known that they are also present in aquatic environments, such as freshwater lakes ( 27 ), sediments ( 22 , 28 – 30 ), and estuaries ( 31 , 32 ). In addition, G. phototrophica was isolated from a freshwater lake in Inner Mongolia ( 18 ).…”

Section: Introductionmentioning

confidence: 99%

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Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes

et al. 2021

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Members of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. Sequences affiliated with Gemmatimonadota were also reported from diverse aquatic habitats; however, it remains unknown whether they are native organisms or represent bacteria passively transported from sediment or soil. To address this question, we analyzed metagenomes constructed from five freshwater lakes in central Europe. Based on the 16S rRNA gene frequency, Gemmatimonadota represented from 0.02 to 0.6% of all bacteria in the epilimnion and between 0.1 and 1% in the hypolimnion. These proportions were independently confirmed using catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). Some cells in the epilimnion were attached to diatoms (Fragilaria sp.) or cyanobacteria (Microcystis sp.), which suggests a close association with phytoplankton. In addition, we reconstructed 45 metagenome-assembled genomes (MAGs) related to Gemmatimonadota. They represent several novel lineages, which persist in the studied lakes during the seasons. Three lineages contained photosynthesis gene clusters. One of these lineages was related to Gemmatimonas phototrophica and represented the majority of Gemmatimonadota retrieved from the lakes’ epilimnion. The other two lineages came from hypolimnion and probably represented novel photoheterotrophic genera. None of these phototrophic MAGs contained genes for carbon fixation. Since most of the identified MAGs were present during the whole year and cells associated with phytoplankton were observed, we conclude that they represent truly limnic Gemmatimonadota distinct from the previously described species isolated from soils or sediments. IMPORTANCE Photoheterotrophic bacterial phyla such as Gemmatimonadota are key components of many natural environments. Its first photoheterotrophic cultured member, Gemmatimonas phototrophica, was isolated in 2014 from a shallow lake in the Gobi Desert. It contains a unique type of photosynthetic complex encoded by a set of genes which were likely received via horizontal transfer from Proteobacteria. We were intrigued to discover how widespread this group is in the natural environment. In the presented study, we analyzed 45 metagenome-assembled genomes (MAGs) that were obtained from five freshwater lakes in Switzerland and Czechia. Interestingly, it was found that phototrophic Gemmatimonadota are relatively common in euphotic zones of the studied lakes, whereas heterotrophic Gemmatimonadota prevail in deeper waters. Moreover, our analysis of the MAGs documented that these freshwater species contain almost the same set of photosynthesis genes identified before in Gemmatimonas phototrophica originating from the Gobi Desert.

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Section: Discussionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes

et al. 2021

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“…The higher light intensity in OL and OL-Inh treatments compared to LL treatment could favor photoheterotrophic bacteria, such as AAP bacteria, whose growth efficiency has been documented to be enhanced by light both in the laboratory and in marine waters (26,27,41). In agreement with this assumption, proteobacterial ASVs in the total bacterial community affiliated with genera known to contain AAP bacterial species, such as Limnohabitans, Polynucleobacter (Burkholderiales), and Roseomonas (Rhodospirillalles) (31,44), were also found to be relatively abundant members of the AAP community ( Fig. 4B and 5B).…”

Section: Discussionmentioning

confidence: 59%

“…S4B) indicates that some "bottle effect" may have occurred. On the other hand, Verrucomicrobiota and Alphaproteobacteria (including the order Caulobacterales), which showed the highest increase in relative abundance throughout the experiment, were reported to be the most active groups based on 16S rRNA amplicon libraries constructed from the transcript in a mesocosm experiment conducted at the same time in the Ř ímov Reservoir (44). Thus, although we were not able to completely exclude the "bottle effect" from our enclosures, we conclude that the observed changes in total bacterial and AAP communities resulted predominantly from their response to the manipulation of primary production and less from the "bottle effect" per se.…”

Section: Discussionmentioning

confidence: 99%

“…The filters were dried of excess water by gently pressing in a paper towel, and pigments were immediately extracted in acetone-methanol mixture (7:2 [vol/vol], high-pressure liquid chromatography [HPLC] grade; Penta, Prague, Czechia). Clear extracts were analyzed by using a Prominence-i HPLC system (Shimadzu, Kyoto, Japan) as described previously (44).…”

Section: Methodsmentioning

confidence: 99%

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Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

Piwosz

Vrdoljak

Frenken

et al. 2020

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Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions. IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.

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