Heterotrophic Bacteria Enhance the Aggregation of the Marine Picocyanobacteria Prochlorococcus and Synechococcus

Abstract

Marine picocyanobacteria are ubiquitous primary producers across the world’s oceans, and play a key role in the global carbon cycle. Recent evidence stemming from in situ investigations have shown that picocyanobacteria are able to sink out of the euphotic zone to depth, which has traditionally been associated with larger, mineral ballasted cells. The mechanisms behind the sinking of picocyanobacteria remain a point of contention, given that they are too small to sink on their own. To gain a mechanistic understanding of the potential role of picocyanobacteria in carbon export, we tested their ability to form “suspended” (5–60 μm) and “visible” (ca. > 0.1 mm) aggregates, as well as their production of transparent exopolymer particles (TEP)—which are a key component in the formation of marine aggregates. Additionally, we investigated if interactions with heterotrophic bacteria play a role in TEP production and aggregation in Prochlorococcus and Synechococcus by comparing xenic and axenic cultures. We observed TEP production and aggregation in batch cultures of axenic Synechococcus , but not in axenic Prochlorococcus . Heterotrophic bacteria enhanced TEP production as well as suspended and visible aggregate formation in Prochlorococcus , while in Synechococcus , aggregation was enhanced with no changes in TEP. Aggregation experiments using a natural plankton community dominated by picocyanobacteria resulted in aggregation only in the presence of the ballasting mineral kaolinite, and only when Synechococcus were in their highest seasonal abundance. Our results point to a different export potential between the two picocyanobacteria, which may be mediated by interactions with heterotrophic bacteria and presence of ballasting minerals. Further studies are needed to clarify the mechanistic role of bacteria in TEP production and aggregation of these picocyanobacteria.

Microplastics increase the marine production of particulate forms of organic matter

“…This suggests that biological production and rapid aggregation of organic gels are a possible removal mechanism of microplastics from the water column, supporting recent observations (Kaiser et al 2017, Michels et al 2018. The presence of both heterotrophic bacteria and suspended particles may increase the stickiness of Synechococcus-derived TEP or its precursors, enhancing cell aggregation and export (Deng et al 2015, Cruz andNeuer 2019). Bacteria can also release TEP or TEP precursors, which result in stickier particles, richer in uronic acids (Bhaskar et al 2005).…”

“…Synechococcus is a widespread cyanobacteria group and a high TEP producer (Ortega-Retuerta et al 2019, Zamanillo et al 2019) that contributes to carbon export in many areas of the ocean thanks to its capacity to form large aggregates (Cruz and Neuer 2019). Our results suggest that inert polystyrene microplastics act the same way as inorganic ballasting particles to favor an increased metabolism and interaction of both autotrophic (Synechococcus) and heterotrophic bacteria.…”

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

“…69504) following manufacturer instructions. The V4-V5 region of the 16S rRNA gene was ampli ed using the 515F-Y (5'-GTGYCAGCMGCCGCGGTAA-3') and 926R (5'-CCGYCAATTYMTTTRAGTT-3') primers (Parada et al, 2016), and sequencing libraries prepared in duplicate before pooling using a two-step protocol described previously (25), with the exception of the MED4, NATL2A, and MIT9313 cultures from 2018, which used the same two-step protocol, but were generated in a different sequencing run using 515F (5'-GTGCCAGCMGCCGCGGTAA-3') and 806R (5'-GGACTACHVGGGTWTCTAAT-3') primers (Preheim et al, 2013). The libraries were sequenced on an Illumina MiSeq (Illumina, San Diego, CA, USA) platform, using 250 bp paired-end reads (except for the 2018 MED4, NATL2A, and MIT9313 cultures, which used 150 bp paired-end reads).…”

“…Given the small size of picocyanobacteria, cells that attach directly to the picocyanobacterial host (apparent for some Synechococcus (Malfatti & Azam, 2009)) or associate with them in particulate matter (e.g. through heterotroph-mediated aggregation of cyanobacteria (Cruz & Neuer, 2019)) would be spatially co-localized enough to experience a so-called "phycosphere".…”

Assessing the Temporal Variability and Drivers of Transparent Exopolymer Particle Concentrations and Production Rates in a Subtropical Estuary

“…Heterotrophic bacteria are tightly coupled with phytoplankton and respond rapidly to transient shifts in coastal phytoplankton communities, turning over phytoplankton-derived organic matter that drives ecosystem-wide biogeochemistry (Buchan et al 2014). Previous literature has suggested that bacteria may produce extracellular polymeric substances that can form TEP (Passow 2002b;Ortega-Retuerta et al 2010), while others have noted that bacteria may indirectly influence TEP production, via the release of enzymes that promote particle aggregation in closely associated phytoplankton (Gärdes et al 2011;Cruz and Neuer 2019). Production of bacterially derived TEP may help to explain several patterns in our data, including the discrepancy between the high TEP concentrations and low TEP to chlorophyll ratio observed at high tide, as well as the similar diel pattern observed between TEP concentrations and the TEP to chlorophyll ratio.…”