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Proteorhodopsin Phototrophy in Antarctic Coastal Waters.

ABSTRACT: Microbial proton-pumping rhodopsins are considered the simplest strategy among phototrophs to conserve energy from light. Proteorhodopsins are the most studied rhodopsins thus far because of their ubiquitous presence in the ocean, except in Antarctica, where they remain understudied. We analyzed proteorhodopsin abundance and transcriptional activity in the Western Antarctic coastal seawaters. Combining quantitative PCR (qPCR) and metagenomics, the relative abundance of proteorhodopsin-bearing bacteria accounted on average for 17, 3.5, and 29.7% of the bacterial community in Chile Bay (South Shetland Islands) during 2014, 2016, and 2017 summer-autumn, respectively. The abundance of proteorhodopsin-bearing bacteria changed in relation to environmental conditions such as chlorophyll a and temperature. Alphaproteobacteria, Gammaproteobacteria, and Flavobacteriia were the main bacteria that transcribed the proteorhodopsin gene during day and night. Although green light-absorbing proteorhodopsin genes were more abundant than blue-absorbing ones, the latter were transcribed more intensely, resulting in >50% of the proteorhodopsin transcripts during the day and night. Flavobacteriia were the most abundant proteorhodopsin-bearing bacteria in the metagenomes; however, Alphaproteobacteria and Gammaproteobacteria were more represented in the metatranscriptomes, with qPCR quantification suggesting the dominance of the active SAR11 clade. Our results show that proteorhodopsin-bearing bacteria are prevalent in Antarctic coastal waters in late austral summer and early autumn, and their ecological relevance needs to be elucidated to better understand how sunlight energy is used in this marine ecosystem. IMPORTANCE Proteorhodopsin-bearing microorganisms in the Southern Ocean have been overlooked since their discovery in 2000. The present study identify taxonomy and quantify the relative abundance of proteorhodopsin-bearing bacteria and proteorhodopsin gene transcription in the West Antarctic Peninsula's coastal waters. This information is crucial to understand better how sunlight enters this marine environment through alternative ways unrelated to chlorophyll-based strategies. The relative abundance of proteorhodopsin-bearing bacteria seems to be related to environmental parameters (e.g., chlorophyll a, temperature) that change yearly at the coastal water of the West Antarctic Peninsula during the austral late summers and early autumns. Proteorhodopsin-bearing bacteria from Antarctic coastal waters are potentially able to exploit both the green and blue spectrum of sunlight and are a prevalent group during the summer in this polar environment.

SUBMITTER: Cifuentes-Anticevic J

PROVIDER: S-EPMC8386455 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:A metaproteomic survey of surface coastal waters near Palmer Station on the Antarctic Peninsula, West Antarctica, was performed, revealing marked differences in the functional capacity of summer and winter communities of bacterioplankton. Proteins from Flavobacteria were more abundant in the summer metaproteome, whereas winter was characterized by proteins from ammonia-oxidizing Marine Group I Crenarchaeota. Proteins prevalent in both seasons were from SAR11 and Rhodobacterales clades of Alphaproteobacteria, as well as many lineages of Gammaproteobacteria. The metaproteome data were used to elucidate the main metabolic and energy generation pathways and transport processes occurring at the microbial level in each season. In summer, autotrophic carbon assimilation appears to be driven by oxygenic photoautotrophy, consistent with high light availability and intensity. In contrast, during the dark polar winter, the metaproteome supported the occurrence of chemolithoautotrophy via the 3-hydroxypropionate/4-hydroxybutyrate cycle and the reverse tricarboxylic acid cycle of ammonia-oxidizing archaea and nitrite-oxidizing bacteria, respectively. Proteins involved in nitrification were also detected in the metaproteome. Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that 'dark' carbon fixation has in winter.

Project description:The marine ecosystem along the Western Antarctic Peninsula undergoes a dramatic seasonal transition every spring, from almost total darkness to almost continuous sunlight, resulting in a cascade of environmental changes, including phytoplankton blooms that support a highly productive food web. Despite having important implications for the movement of energy and materials through this ecosystem, little is known about how these changes impact bacterial succession in this region. Using 16S rRNA gene amplicon sequencing, we measured changes in free-living bacterial community composition and richness during a 9-month period that spanned winter to the end of summer. Chlorophyll a concentrations were relatively low until summer when a major phytoplankton bloom occurred, followed 3 weeks later by a high peak in bacterial production. Richness in bacterial communities varied between ~1,200 and 1,800 observed operational taxonomic units (OTUs) before the major phytoplankton bloom (out of ~43,000 sequences per sample). During peak bacterial production, OTU richness decreased to ~700 OTUs. The significant decrease in OTU richness only lasted a few weeks, after which time OTU richness increased again as bacterial production declined toward pre-bloom levels. OTU richness was negatively correlated with bacterial production and chlorophyll a concentrations. Unlike the temporal pattern in OTU richness, community composition changed from winter to spring, prior to onset of the summer phytoplankton bloom. Community composition continued to change during the phytoplankton bloom, with increased relative abundance of several taxa associated with phytoplankton blooms, particularly Polaribacter. Bacterial community composition began to revert toward pre-bloom conditions as bacterial production declined. Overall, our findings clearly demonstrate the temporal relationship between phytoplankton blooms and seasonal succession in bacterial growth and community composition. Our study highlights the importance of high-resolution time series sampling, especially during the relatively under-sampled Antarctic winter and spring, which enabled us to discover seasonal changes in bacterial community composition that preceded the summertime phytoplankton bloom.

Project description:Understanding underwater optics in natural waters is essential in evaluating aquatic primary production and risk of UV exposure in aquatic habitats. Changing environmental conditions related with global climate change, which imply potential contrasting changes in underwater light climate further emphasize the need to gain insights into patterns related with underwater optics for more accurate future predictions. The present study evaluated penetration of solar radiation in six sub-Antarctic estuaries and fjords in Chilean North Patagonian region (39-44°S) and in an Antarctic bay (62°S). Based on vertical diffuse attenuation coefficients (Kd), derived from measurements with a submersible multichannel radiometer, average summer UV penetration depth (z1%) in these water bodies ranged 2-11 m for UV-B (313 nm), 4-27 m for UV-A (395 nm), and 7-30 m for PAR (euphotic zone). UV attenuation was strongest in the shallow Quempillén estuary, while Fildes Bay (Antarctica) exhibited the highest transparency. Optically non-homogeneous water layers and seasonal variation in transparency (lower in winter) characterized Comau Fjord and Puyuhuapi Channel. In general, multivariate analysis based on Kd values of UV and PAR wavelengths discriminated strongly Quempillén estuary and Puyuhuapi Channel from other study sites. Spatial (horizontal) variation within the estuary of Valdivia river reflected stronger attenuation in zones receiving river impact, while within Fildes Bay a lower spatial variation in water transparency could in general be related to closeness of glaciers, likely due to increased turbidity through ice-driven processes. Higher transparency and deeper UV-B penetration in proportion to UV-A/visible wavelengths observed in Fildes Bay suggests a higher risk for Antarctic ecosystems reflected by e.g. altered UV-B damage vs. photorepair under UV-A/PAR. Considering that damage repair processes often slow down under cool temperatures, adverse UV impact could be further exacerbated by cold temperatures in this location, together with episodes of ozone depletion. Overall, the results emphasize the marked spatial (horizontal and vertical) and temporal heterogeneity of optical characteristics, and challenges that these imply for estimations of underwater optics.

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Proteorhodopsin Phototrophy in Antarctic Coastal Waters.

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