Comparative membrane proteomics reveal contrasting adaptation strategies for coastal and oceanic marine Synechococcus cyanobacteria

Abstract

Marine cyanobacteria genus Synechococcus are among the most abundant and widespread primary producers in the open ocean. Synechococcus strains belonging to different clades have adapted distinct strategies for growth and survival across a range of marine conditions. Clades I and IV are prevalent in colder, mesotrophic, coastal waters, while clades II and III prefer warm, oligotrophic open oceans. To gain insight into the cellular resources these unicellular organisms invest in adaptation strategies we performed shotgun membrane proteomics of four Synechococcus spp. strains namely CC9311 (clade I), CC9605 (clade II), WH8102 (clade III) and CC9902 (clade IV). Comparative membrane proteomes analysis demonstrated that CC9902 and WH8102 showed high resource allocation for phosphate uptake, accounting for 44% and 38% of overall transporter protein expression of the species. WH8102 showed high expression of the iron uptake ATP-binding cassette binding protein FutA, suggesting that a high binding affinity for iron is possibly a key adaptation strategy for some strains in oligotrophic ocean environments. One protein annotated as a phosphatase 2c (Sync_2505 and Syncc9902_0387) was highly expressed in the coastal mesotrophic strains CC9311 and CC9902, constituting 14%-16% of total membrane protein, indicating a vital, but undefined function, for strains living in temperate mesotrophic environments.

Intraspecific trait variation modulates the temperature effect on elemental quotas and stoichiometry in marine Synechococcus

“…The four Synechococcus strains differ in their background in terms of adaptation to environmental nutrients, and have distinctive thermal ranges. CC9902 and CC9311 are both mesotrophic strains of Synechococcus , adapted to higher concentrations of phosphorus and iron, yet have very distinct physiological responses, which suggests the role of strain is greater than that of adaptation to environmental nutrients in determining environmental responses ( Table 1 ) [ 42 , 44 , 47 , 49 ]. This becomes more pronounced as BL107 is an oligotrophic strain, yet its cell size and elemental quotas more closely resemble those of CC9902 (Figs 3 – 6 ).…”

“…The strains used during experimentation are presented here, with additional information such as clade, location of isolation, isolation depth, previously reported temperature optimum, our experimentally observed thermal optimum, previously reported thermal ranges, our experimentally observed range in cell size, our experimentally observed mean cell size, growth in oligotrophic conditions, iron conditions, light acclimation pigment types and operons, and phosphate adaptation provided. High Fe [42,44] 3da (mpeBA) [45] High [44] BL107 IV [39,43] Balearic Sea [39] 1800 m 24˚C [46] 22˚C…”

Functional characterisation of substrate-binding proteins to address nutrient uptake in marine picocyanobacteria

“…While this mini-review focusses on picocyanobacterial ABC transporters, other predicted transporters (e.g. permeases, ion channels, tripartite ATP-independent periplasmic transporters) may contribute to the uptake of other nutrients [9,11,21,22]. Studies have sought to assess whether changes in gene content among major lineages can provide insight into the global patterns of picocyanobacterial resource use [10,[23][24][25].…”

“…Notably, omics-based platforms offer an unparalleled capacity to identify patterns of nutrient adaptation [ 22 , 25 , 30 , 31 ], including alternative metabolic strategies (mixotrophy), in picocyanobacteria [ 25 , 32 , 33 ]. Such approaches fundamentally depend on precise functional annotations of cellular nutrient acquisition systems.…”

“…Like urea, additional organic nitrogen uptake may also occur through predicted cyanate transporters (CK_2165). The distribution of these transporters appears clade-specific in Synechococcus (Clade III) [22], however, these are yet to be functionally validated. As nitrogen is a major limiting nutrient in marine environments, mixotrophic strategies for the acquisition of organic nitrogen may be crucial for picocyanobacteria [33,63,[88][89][90].…”