The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics

Abstract

Heterotrophic marine bacteria play key roles in remineralizing organic matter generated from primary production. However, far more is known about which groups are dominant than about the cellular processes they perform in order to become dominant. In the Southern Ocean, eukaryotic phytoplankton are the dominant primary producers. In this study we used metagenomics and metaproteomics to determine how the dominant bacterial and archaeal plankton processed bloom material. We examined the microbial community composition in 14 metagenomes and found that the relative abundance of Flavobacteria (dominated by Polaribacter) was positively correlated with chlorophyll a fluorescence, and the relative abundance of SAR11 was inversely correlated with both fluorescence and Flavobacteria abundance. By performing metaproteomics on the sample with the highest relative abundance of Flavobacteria (Newcomb Bay, East Antarctica) we defined how Flavobacteria attach to and degrade diverse complex organic material, how they make labile compounds available to Alphaproteobacteria (especially SAR11) and Gammaproteobacteria, and how these heterotrophic Proteobacteria target and utilize these nutrients. The presence of methylotrophic proteins for archaea and bacteria also indicated the importance of metabolic specialists. Overall, the study provides functional data for the microbial mechanisms of nutrient cycling at the surface of the coastal Southern Ocean.

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

“…Consequently, Bacteroidetes and phytoplankton are often found in close association in polar waters (Grossart et al, 2005;Piquet et al, 2011;Williams et al, 2013) with the relative abundance of the former significantly correlated with the emergence of the late spring blooms (Alonso-Sáez et al, 2008). During May of 2014, the Flavobacteriaceae were notable by their prolific increase in relative abundance from negligible levels in March, congruent with the spike in chloroplast 16S rRNA abundance (Figure 5) and chl a maxima ( Table 1).…”

“…Recent whole genome analyses of various members of the Bacteroidetes have confirmed long-held assumptions of a preference for and selective advantage of the phylum when growing on complex organic matter (Abell and Bowman, 2005;Teeling et al, 2012;Fernández-Gómez et al, 2013;Williams et al, 2013), such as that typically produced by marine phytoplankton (Passow, 2002). Consequently, Bacteroidetes and phytoplankton are often found in close association in polar waters (Grossart et al, 2005;Piquet et al, 2011;Williams et al, 2013) with the relative abundance of the former significantly correlated with the emergence of the late spring blooms (Alonso-Sáez et al, 2008).…”

“…By late summer, this develops into a successional postbloom stage, comprising different phytoplankton populations (Sherr et al, 2003) and it follows, their different associated successional heterotrophic prokaryote consortia, in particular the Flavobacteriia and Gammaproteobacteria classes (AlonsoSáez et al, 2008;Teeling et al, 2012). This phenomenon of the polar phytoplankton blooms (Williams et al, 2013) followed by the heterotrophic bacterial populations also seemingly drives the annual disappearance of the chemolithoautotrophic marine Archaea from surface waters (Kalanetra et al, 2009;AlonsoSáez et al, 2012;Pedneault et al, 2014) and the subsequent seasonal fluctuations in prokaryote diversity (Murray et al, 1998;Ghiglione and Murray, 2012;Grzymski et al, 2012;Ladau et al, 2013).…”

Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects

“…Surface waters (AZ, Polar Frontal Zone (PFZ) and SAMW) had high abundances of OTUs clustering with SILVA sequences from the Alphaproteobacteria, Bacteroidetes and Gammaproteobacteria. The higher abundance of Bacteroidetes at the surface reflects their association with phytoplankton, as many species in this lineage specialize in the degradation of high molecular weight products of primary production 20 . Alphaproteobacteria were represented primarily by the SAR11 clade, abundant in ocean surface communities 21 including the SO 22 , and Roseobacter clades, which have also been associated with degradation of phytoplankton products 15,20 (Supplementary Data 2).…”

“…The higher abundance of Bacteroidetes at the surface reflects their association with phytoplankton, as many species in this lineage specialize in the degradation of high molecular weight products of primary production 20 . Alphaproteobacteria were represented primarily by the SAR11 clade, abundant in ocean surface communities 21 including the SO 22 , and Roseobacter clades, which have also been associated with degradation of phytoplankton products 15,20 (Supplementary Data 2). The dominant Gammaproteobacterial orders were the Alteromonadales and Oceanospirillales, typical of SO surface waters 23 .…”