Broad phylogenetic and functional diversity among mixotrophic consumers of Prochlorococcus

Abstract

Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty-nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2–5 µm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten-fold across isolates and six-fold across genera. Slower grazers tended to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76–250 cells mL−1 across depths in the upper euphotic zone (5–100 m). Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.

Trophic strategies explain the ocean niches of small eukaryotic phytoplankton

“…The latter pattern appears to contradict the current results, but it could be consistent if the increase in mixotroph abundance in coastal waters was driven by the relatively autotrophic dictyochophyte Florenciella. This genus is globally abundant (17), grazes relatively slowly (17) (Fig. 2), grows quickly on dissolved nutrients (35) (Fig.…”

“…The remaining seven strains can grow phagotrophically (Fig. S2, (17)), and the rates at which they ingest Prochlorococcus were previously reported (17). To characterize how phagotrophic capacity is related to phototrophy we measured growth of all strains under phototrophic conditions (addition of dissolved nutrients but not prey) at a 'high' irradiance (100 µmol photons m -2 s -1 ) that is the typical optimal irradiance for phytoplankton growth (27) and a 'low' irradiance (10 µmol photons m -2 s -1 ) that is ~1% of surface PAR at the location from which these strains were isolated (32).…”

“…Isolation methods for most strains used in this study were described in Li et al (17). Briefly, the majority were isolated from the euphotic zone at Station ALOHA (22°45' N, 158°00' W) in 2019, enriched using Keller (K) medium with a 20-fold reduction in mineral nutrients and addition of Prochlorococcus (MIT9301) at ~5×10 6 cells mL -1 .…”

“…Habitat differences among clades suggest functional diversity (12)(13)(14), but understanding how key traits vary is hampered by a paucity of experiments on isolates, especially those cultivated from the open ocean (3,15,16). Trophic strategy may be an important axis of divergence: most taxa include phagotrophic mixotrophs that make their own chloroplasts (6,17), and feeding rates vary across clades (17), but groups such as non-flagellated prasinophytes likely cannot ingest prey, and this may be true of some flagellates as well (18,19). Thus there is likely a spectrum of trophic strategies, ranging from strictly autotrophic to largely heterotrophic phytoplankton, but data on how key functions vary across species and communities is lacking.…”

“…The strains previously shown to grow when fed Prochlorococcus (Chrysochromulina (1), Chrysochromulina (2), and ChrysoH) increased relative to control cultures (no prey added), while the remaining strains (Ostreococcus, Chloropicon, Micromonas, Pelagomonas) did not. All additional strains used in this study were previously shown to consume Prochlorococcus and grow mixotrophically(17).…”