The Synechococcus cell surface protein SwmA increases vulnerability to predation by flagellates and ciliates

Abstract

The genus Synechococcus, a major contributor to ocean productivity, exhibits wide genetic variability and a distinct biogeography of genetic subgroups. Synechococcus sp. strain WH8102 is a motile Sargasso Sea isolate belonging to Clade III in subcluster 5.1. Non‐flagellar motility in WH8102 depends upon two large cell surface proteins, SwmA and SwmB. In the marine plankton, Synechococcus can experience high rates of mortality from protist predators, suggesting strong selective pressure for the maintenance of anti‐predation defenses. We used knockout mutants deficient in large cell surface proteins (SwmA‐ and SwmB‐) to test the hypothesis that these proteins defend WH8102 against predation by ciliates and flagellates, important consumers of Synechococcus in aquatic ecosystems. Contrary to our hypothesis, we found that wild‐type WH8102 were preyed upon at higher rates than SwmA‐ by ciliates and by two of three tested flagellate species. Thus the SwmA protein, constitutively produced by WH8102, made this strain more rather than less vulnerable to predation. SwmA proteins link to form the S layer, a cell coating known to promote adhesion in other microbial systems, suggesting the predation vulnerability arises from increased attachment between consumers and prey. Given the SwmA‐related enhancement of predation rates, our findings suggest two possibilities for WH8102 and perhaps other Clade III Synechococcus: (1) factors other than protist predation select for production of the S layer; (2) ingestion actually increases fitness, by exposing digestion‐resistant cells to beneficial conditions in the food vacuole.

Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa

“…We also found similar heterogeneity between isolates collected in 2011 and 2013 despite differences in culturing time. Further supporting an increased occurrence of genomic heterogeneity among LL/LG colonies, we found increased frequencies of genes in LL/LG genomes that may facilitate nonclonal colony formation: (a) NeuB that synthesizes sialic acids, which are a component of cyanobacterial extracellular polymeric substances (Strom, Bright, Fredrickson, & Brahamsha, 2017;Zippel & Neu, 2011) and play important roles in cellular recognition and adhesion (Gunawan et al, 2005); (b) sialidases that may facilitate cellular adhesion by uncovering carbohydrate receptors that are recognized by bacterial adhesins (Vimr, 1994);…”

“…We also found similar heterogeneity between isolates collected in 2011 and 2013 despite differences in culturing time. Further supporting an increased occurrence of genomic heterogeneity among LL/LG colonies, we found increased frequencies of genes in LL/LG genomes that may facilitate nonclonal colony formation: (a) NeuB that synthesizes sialic acids, which are a component of cyanobacterial extracellular polymeric substances (Strom, Bright, Fredrickson, & Brahamsha, ; Zippel & Neu, ) and play important roles in cellular recognition and adhesion (Gunawan et al, ); (b) sialidases that may facilitate cellular adhesion by uncovering carbohydrate receptors that are recognized by bacterial adhesins (Vimr, ); (c) pfam06229 (FRG1‐like domain) that contains a Hydra spp. gene linked to this freshwater cnidarian's ability to adhere to underwater surfaces (Rodrigues et al, ); and (d) a bacterial adhesin (pfam03865: haemolysin secretion/activation protein ShlB/FhaC/HecB) (Moslavac et al, ) that facilitates adhesion to other cells in pathogenic and symbiotic interactions (Hooper & Gordon, ).…”

18S rRNA gene sequences of leptocephalus gut contents, particulate organic matter, and biological oceanographic conditions in the western North Pacific

“…Additionally, Prochlorococcus may be important as a food source because they are present at high levels in the SCM. The cell membranes of Prochlorococcus are covered with proteins 59 and release monosaccharides 60 , the extracellular exudates are composed of low-molecular-weight compounds 61 , and the extracellular vesicles contain rich nutrients such as lipids, proteins, and nucleic acids 62 , 63 . In seawater, it is known that transparent exopolymer particles (TEPs) exist and are mixed with a substantial amount of protein-rich amorphous particles 64 – 66 .…”

Factors Affecting the Mixotrophic Flagellate Poterioochromonas malhamensis Grazing on Chlorella Cells

“…; Strom et al. ), food nutritional quality (John and Davidson ; Shannon et al. ; Siuda and Dam ), and physiology of the prey (Verhagen et al.…”

“…Grazing selectivity is influenced by various factors including the growth environment and the morphological and physiological features of the prey (Ng et al 2017). In fact, many factors, for example prey size (Hansen 1992;Jakobsen and Hansen 1997;Jakobsen and Tang 2002), prey motility (Boenigk et al 2001;Buskey 1997), biochemical composition of prey (Ng et al 2017), surface structure variation in prey (Monger et al 1999;Strom et al 2017), food nutritional quality (John and Davidson 2001;Shannon et al 2007;Siuda and Dam 2010), and physiology of the prey (Verhagen et al 1993), have been reported to influence the feeding behaviour of protozoa on algal prey. Knowledge of the interaction between protozoa and phytoplankton is very helpful in interpreting how the underlying mechanisms drive feeding selectivity in planktonic protists (Roberts et al 2011;Strom 2002); however, compared with other groups, considerably less attention has been paid to mixotrophic flagellates by experimental ecologists (Esteban et al 2010;Tillmann 2004).…”