Seasonal assemblages and short‐lived blooms in coastal north‐west Atlantic Ocean bacterioplankton

Abstract

Temperate oceans are inhabited by diverse and temporally dynamic bacterioplankton communities. However, the role of the environment, resources and phytoplankton dynamics in shaping marine bacterioplankton communities at different time scales remains poorly constrained. Here, we combined time series observations (time scales of weeks to years) with molecular analysis of formalin-fixed samples from a coastal inlet of the north-west Atlantic Ocean to show that a combination of temperature, nitrate, small phytoplankton and Synechococcus abundances are best predictors for annual bacterioplankton community variability, explaining 38% of the variation. Using Bayesian mixed modelling, we identified assemblages of co-occurring bacteria associated with different seasonal periods, including the spring bloom (e.g. Polaribacter, Ulvibacter, Alteromonadales and ARCTIC96B-16) and the autumn bloom (e.g. OM42, OM25, OM38 and Arctic96A-1 clades of Alphaproteobacteria, and SAR86, OM60 and SAR92 clades of Gammaproteobacteria). Community variability over spring bloom development was best explained by silicate (32%)--an indication of rapid succession of bacterial taxa in response to diatom biomass--while nanophytoplankton as well as picophytoplankton abundance explained community variability (16-27%) over the transition into and out of the autumn bloom. Moreover, the seasonal structure was punctuated with short-lived blooms of rare bacteria including the KSA-1 clade of Sphingobacteria related to aromatic hydrocarbon-degrading bacteria.

Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year

“…The nitrite-oxidizing genus Nitrospina has been observed in winter-only samples from both Antarctic (Grzymski et al, 2012) and Arctic (Alonso-Sáez et al, 2010) waters, as well as in temperate waters (El-Swais et al, 2015) and has also been correlated with amoA-containing Thaumarchaeota in Monterey Bay (Mincer et al, 2007). Whilst we recorded generally higher levels of all three taxa in winter surface and year-round deeper waters, active populations were still detected in surface waters in summer months, albeit at much lower levels.…”

“…We observed distinct seasonal fluctuations in prokaryote diversity, comprising high richness in the darker autumn and winter months and lower richness in the late spring and summer (Gilbert et al, 2012;El-Swais et al, 2015), similar to other surveys of surface waters in high latitude marine ecosystems (Murray et al, 1998;Murray and Grzymski, 2007;Ghiglione and Murray, 2012;Grzymski et al, 2012;Ladau et al, 2013). Phylotype richness peaked in January and then decreased through the year (Figure 4) until the annual minimum in August, coincident with the late summer phytoplankton post-bloom, before increasing again in the late autumn.…”

“…In our study, the Proteobacteria were the most abundant bacterial phylum throughout the year and of these, it was the class Gammaproteobacteria that predominated, particularly in the summer months, along with class Flavobacteriia of the phylum Bacteroidetes (Figure 2). The high relative abundance of these taxa in coastal waters around Svalbard (Zeng et al, 2013) has been associated with the release of dissolved organic matter following a phytoplankton bloom (Ghiglione and Murray, 2012;De Corte et al, 2013;Buchan et al, 2014;El-Swais et al, 2015) and they are seen to dominate Arctic MYI communities (Bowman et al, 2012). The Gammaproteobacteria are typically seen to increase toward the summer months (Alonso-Sáez et al, 2008) and of the strong indicator phylotypes determined during the study year, three of the top five (Oceanospirillaceae, Halomondaceae and Alteromonadaceae) were members of this class (Figure 5).…”

“…The Gammaproteobacteria are typically seen to increase toward the summer months (Alonso-Sáez et al, 2008) and of the strong indicator phylotypes determined during the study year, three of the top five (Oceanospirillaceae, Halomondaceae and Alteromonadaceae) were members of this class (Figure 5). Members of both the Oceanospirillaceae and Alteromonadaceae are known to be r-strategist, broad substrate generalists and are frequently seen to be closely-associated with phytoplankton blooms (Teeling et al, 2012;Buchan et al, 2014;El-Swais et al, 2015). However, in comparison with the abundance of physiological and genomic studies of bloom-associated Bacteroidetes and Alphaproteobacteria strains, there is a relative paucity of data regarding the Gammaproteobacteria (Buchan et al, 2014).…”

“…Unmitigated atmospheric warming will undoubtedly affect gross changes in the marine environment and its phytoplankton populations through increased photoirradiation and nutrients made available by thawing sea ice and permafrost Doney et al, 2012;El-Swais et al, 2015), respectively. Whilst the phytoplankton blooms are restricted to the well-lit upper layers of the ocean, the effects of their prolific but short-lived activity are seen throughout the deep ocean beneath.…”