Seasonal niche differentiation among closely related marine bacteria

Abstract

Bacteria display dynamic abundance fluctuations over time in marine environments, where they play key biogeochemical roles. Here, we characterized the seasonal dynamics of marine bacteria in a coastal oligotrophic time series station, tested how similar the temporal niche of closely related taxa is, and what are the environmental parameters modulating their seasonal abundance patterns. We further explored how conserved the niche is at higher taxonomic levels. The community presented recurrent patterns of seasonality for 297 out of 6825 amplicon sequence variants (ASVs), which constituted almost half of the total relative abundance (47%). For certain genera, niche similarity decreased as nucleotide divergence in the 16S rRNA gene increased, a pattern compatible with the selection of similar taxa through environmental filtering. Additionally, we observed evidence of seasonal differentiation within various genera as seen by the distinct seasonal patterns of closely related taxa. At broader taxonomic levels, coherent seasonal trends did not exist at the class level, while the order and family ranks depended on the patterns that existed at the genus level. This study identifies the coexistence of closely related taxa for some bacterial groups and seasonal differentiation for others in a coastal marine environment subjected to a strong seasonality.

Spatiotemporal Variation of Microbial Communities in the Ultra-Oligotrophic Eastern Mediterranean Sea

“…The recurrent shifts in microbial structure and activity followed typical seasonal patterns. Physical mixing of the water column in early winter seemed to be responsible for a “resetting” of the microbial ecosystem from a low diversity state in summer, when the microbial community in the EMS is nutrient depleted ( Thingstad et al, 2005 ; Tanaka et al, 2011 ; Ben Ezra et al, 2021 ), to a high diversity state in winter, as previously proposed for the Northwestern Mediterranean Sea ( Salter et al, 2015 ; Auladell et al, 2021 ). Our two early winter cruises showed differences in some environmental parameters such as temperature and fluorescence ( Supplementary Table S5 ) pointing to different mixing conditions.…”

“…The observed abundance of the dominant group, SAR11, throughout the year is consistent with data reported for oligotrophic ocean gyres ( Carlson et al, 2009 ; Eiler et al, 2009 ; Morris et al, 2012 ; West et al, 2016 ) though high SAR11 abundances have also been reported from surface waters of offshore stations in the oligotrophic Southern Adriatic Sea ( Korlević et al, 2015 ; see Supplementary Table S9 for a comparison of Mediterranean and open ocean abundances). SAR11 relative abundances at our most coastal station 1 were higher (36%–42% of DNA reads in spring and summer) than those found at coastal stations in other parts of the Mediterranean Sea, including the Northwestern Mediterranean, Southern Mediterranean, and the Adriatic Sea ( Alonso-Sáez et al, 2007 ; Tinta et al, 2015 ; Quéméneur et al, 2020 ; Auladell et al, 2021 ; see Supplementary Table S9 ), highlighting the overall more oligotrophic status of the South Eastern Levantine basin even close to the coast.…”

“…To analyze which ESVs dominate the community and whether dominant and rare ESVs show different patterns, we classified ESVs into four categories broadly following the categories in Auladell et al (2021) : dominant (present in ≥75% of the samples with ≥1% relative abundance), rare (always <1%), intermediate persistent (present in ≥75% of samples), and intermediate fluctuating (present in <75% of samples). Despite the large influence of season on the microbial community, the microbial community structure was dominated by only a few bacterial ESVs throughout the year ( Table 1 ).…”

“…Marine microbial communities play a pivotal function in the ocean’s biogeochemistry because of their key roles in the carbon, nitrogen, and sulfur cycles ( Falkowski et al, 2008 ). Their composition is strongly affected by seasons with recurring microbial turnover over different years, as revealed by oceanographic time-series studies conducted both at offshore stations [e.g., Bermuda Atlantic Time-Series Study (BATS) in the Western Atlantic Ocean and the Hawaii Ocean Time-series (HOTS) in the North Pacific subtropical gyre; Giovannoni and Vergin, 2012 ] and more coastal affected sites [e.g., the San Pedro Ocean Time Series (SPOTS) in the Southern California Bight: Fuhrman et al, 2006 ; the western English Channel: Gilbert et al, 2012 ; and the Northwestern Mediterranean Sea: Galand et al, 2018 ; Auladell et al, 2021 ]. In addition, spatial variability of marine surface water microbial communities has been reported at various scales, ranging from a distance of a few kilometers between sampling sites to samples collected in different ocean basins ( Ghiglione et al, 2005 ; Sunagawa et al, 2015 ; Sebastián et al, 2021 ).…”

Bacterial Indicators Are Ubiquitous Members of Pelagic Microbiome in Anthropogenically Impacted Coastal Ecosystem

“…The core microbiome of our model system comprises Alphaproteobacteria, Bacteroidia, Gammaproteobacteria, and Cyanobacteria as previously reported for coastal marine ecosystems ( Lindh et al, 2015 ; Maresca et al, 2018 ; Pearman et al, 2018 ; Ruiz-González et al, 2019 ; Adyasari et al, 2020 ) and also the Northern Adriatic ( Celussi and Cataletto, 2007 ; Šilović et al, 2012 ; Tinta et al, 2015 ; Paliaga et al, 2017 ; Buccheri et al, 2019 ). Our model ecosystem is strongly subjected to seasonal variations in seawater temperature, solar radiation, weather patterns (winds, freshwater inputs), changes in nutrient availability, stratification, etc., which were recognized as important forcing factors driving seasonal variations in bacterial community structure and function ( Gilbert et al, 2012 ; Fuhrman et al, 2015 ; Auladell et al, 2021 ). Therefore, we conducted in situ surveys in different seasons to be able to distinguish between variations of microbial communities triggered by seasonal variations of abiotic and biotic conditions and those caused by different distance from pollution sources.…”