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

Abstract

AbstractThe 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.