Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria

Ferrera, Isabel; Sánchez, Olga; Kolářová, Eva; Koblížek, Michal; Gasol, Josep M.

doi:10.1038/ismej.2017.79

Cited by 44 publications

(48 citation statements)

References 18 publications

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“…Members of the AAPB family can also utilize various organic and inorganic compounds, perform sulfur oxidation, carbon monoxide oxidation, and produce secondary metabolites [ 60 ]. Light directly affects and stimulates the growth rates and abundance of natural populations of marine AAPB, which explains their abundance in the corals experiencing light pollution at night [ 61 , 62 ]. Anoxygenic phototrophs have previously been detected in the skeletons of the scleractinian corals Montipora monasteriata , Porites cylindrica, and Isopora palifera [ 63 , 64 ].…”

Section: Discussionmentioning

confidence: 99%

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

et al. 2020

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Corals harbor a great diversity of symbiotic microorganisms that play pivotal roles in host nutrition, reproduction, and development. Changes in the ocean environment, such as increasing exposure to artificial light at night (ALAN), may alter these relationships and result in a decline in coral health. In this study, we examined the microbiome associated with gravid specimens of the reef-building coral Acropora digitifera. We also assessed the temporal effects of ALAN on the coral-associated microbial community using high-throughput sequencing of the 16S rRNA gene V4 hypervariable region. The A. digitifera microbial community was dominated by phyla Proteobacteria, Firmicutes, and Bacteroidetes. Exposure to ALAN had no large-scale effect on the coral microbiome, although taxa affiliated with Rhodobacteraceae, Caulobacteraceae, Burkholderiaceae, Lachnospiraceae, and Ruminococcaceae were significantly enriched in corals subjected to ALAN. We further noted an increase in the relative abundance of the family Endozoicomonadaceae (Endozoicomonas) as the spawning period approached, regardless of light treatment. These findings highlight the stability of the A. digitifera microbial community under short-term artificial light pollution and provide initial insights into the response of the collective holobiont to ALAN.

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Section: Discussionmentioning

confidence: 99%

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

et al. 2020

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“…Their discovery challenged previous simplistic views of the structure of ocean microbial food webs [16]. AAP bacteria are relatively common in the euphotic zone of the oceans [17][18][19][20][21], exhibit faster growth rates than other bacterioplankton groups [22,23] and their cells are in general larger than most marine heterotrophic bacteria [24]. Altogether, these characteristics make them relevant in the ecosystem by processing a large amount of organic matter (see review by [15]).…”

Section: Introductionmentioning

confidence: 99%

Long-term seasonal and interannual variability of marine aerobic anoxygenic photoheterotrophic bacteria

Auladell

Sánchez

et al. 2019

The ISME Journal

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We studied the long-term temporal dynamics of the aerobic anoxygenic phototrophic (AAP) bacteria, a relevant functional group in the coastal marine microbial food web, using high-throughput sequencing of the pufM gene coupled with multivariate, time series and co-occurrence analyses at the Blanes Bay Microbial Observatory (NW Mediterranean). Additionally, using metagenomics, we tested whether the used primers captured accurately the seasonality of the most relevant AAP groups. Phylogroup K (Gammaproteobacteria) was the greatest contributor to community structure over all seasons, with phylogroups E and G (Alphaproteobacteria) being prevalent in spring. Diversity indices showed a clear seasonal trend, with maximum values in winter, which was inverse to that of AAP abundance. Multivariate analyses revealed sample clustering by season, with a relevant proportion of the variance explained by day length, temperature, salinity, phototrophic nanoflagellate abundance, chlorophyll a, and silicate concentration. Time series analysis showed robust rhythmic patterns of co-occurrence, but distinct seasonal behaviors within the same phylogroup, and even within different amplicon sequence variants (ASVs) conforming the same operational taxonomic unit (OTU). Altogether, our results picture the AAP assemblage as highly seasonal and recurrent but containing ecotypes showing distinctive temporal niche partitioning, rather than being a cohesive functional group.

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“…Glacier and ice sheet cover 10% of the land surface of the Earth, hosting an enormous diversity of microbes (19), among which the light-driven metabolisms by anoxygenic phototrophs have been proposed to have the potential of significantly influencing glacial carbon fluxes (20). The potential dual phototrophy in glacial bacteria described in this study could further amplify the ecological importance of anoxygenic phototrophs in glacial ecosystems.…”

Section: Ecological Importance and Wide Distribution Of Potential Duamentioning

confidence: 69%

Potential Rhodopsin and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier

Zeng

Chen

Madsen

et al. 2020

Preprint

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Conserving additional energy from sunlight through bacteriochlorophyll (BChl)‐based reaction center or proton‐pumping rhodopsin is a highly successful life strategy in environmental bacteria. Rhodopsin and BChl based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfers (HOT) of the complete gene clusters encoding BChl and xanthorhodopsin (XR)‐based dual phototrophy. Two strains only possess a complete xanthorhodopsin (XR) operon, while the other two strains have both a photosynthesis gene cluster (PGC) and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and located close to a tRNA gene, strongly signaling that a HOT event of XR operon has occurred recently. Mining public genome databases and our High Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl and rhodopsin‐based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy‐deficient environments in surface glaciers, possibly by maximizing the capability of exploiting solar energy.ImportanceOver billions of years of evolution, bacteria capable of light‐driven energy production have occupied every corner of surface Earth where solar irradiation can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light‐harvesting: one is based on the pigment of (bacterio‐)chlorophyll and the other based on light‐sensing retinal molecules. There is emerging genomic evidence that these two rather different systems can co‐exist in a single bacterium to take advantage of their contrasting characteristics in the number of genes involved, biosynthesis cost, ease of expression control and efficiency of energy production, and thus enhance the capability of exploiting solar energy. Our data provide the first clear‐cut evidence that such dual phototrophy potentially exist in glacial bacteria. Further public genome mining suggests this understudied dual phototrophic mechanism is possibly more common than our data alone suggested.Sequence data availabilityGenomes, metagenomes and raw reads were deposited into GenBank under Bioprojects PRJNA548505 and PRJNA552582.

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Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria

Cited by 44 publications

References 18 publications

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

Long-term seasonal and interannual variability of marine aerobic anoxygenic photoheterotrophic bacteria

Potential Rhodopsin and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier

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