The Trichodesmium consortium: conserved heterotrophic co-occurrence and genomic signatures of potential interactions

Abstract

The nitrogen (N)-fixing cyanobacterium Trichodesmium is globally distributed in warm, oligotrophic oceans, where it contributes a substantial proportion of new N and fuels primary production. These photoautotrophs form macroscopic colonies that serve as relatively nutrient-rich substrates that are colonized by many other organisms. The nature of these associations may modulate ocean N and carbon (C) cycling, and can offer insights into marine co-evolutionary mechanisms. Here we integrate multiple omics-based and experimental approaches to investigate Trichodesmium-associated bacterial consortia in both laboratory cultures and natural environmental samples. These efforts have identified the conserved presence of a species of Gammaproteobacteria (Alteromonas macleodii), and enabled the assembly of a near-complete, representative genome. Interorganismal comparative genomics between A. macleodii and Trichodesmium reveal potential interactions that may contribute to the maintenance of this association involving iron and phosphorus acquisition, vitamin B exchange, small C compound catabolism, and detoxification of reactive oxygen species. These results identify what may be a keystone organism within Trichodesmium consortia and support the idea that functional selection has a major role in structuring associated microbial communities. These interactions, along with likely many others, may facilitate Trichodesmium's unique open-ocean lifestyle, and could have broad implications for oligotrophic ecosystems and elemental cycling.

The global Microcystis interactome

“…Similar potential mutualist interactions have recently been mapped between Microcystis and their microbiome of associated bacteria (Xie et al ; Li et al ), corroborating the original idea of a “phycosphere” of functional interaction within the Microcystis aggregates (Bell and Mitchell ; Paerl and Kellar , ; Paerl and Millie ). Moreover, bacteria have been shown to complement algae in marine ecosystems by excreting large amounts of exometabolites including growth factors and biosynthetic precursors, as well as processing toxic metabolites (Morris et al ; Pérez et al ; Lee et al ; Wienhausen et al ). Given the predominance of such data across aquatic system, we hypothesized M. aeruginosa blooms have a microbiome of certain species of associated bacteria or perhaps metabolic functions that will be preserved across geographically distinct Microcystis blooms.…”

The Trichodesmium microbiome can modulate host N2 fixation

“…S1). Notably, similar Gammaproteobacteria are ubiquitously found in association with colonies across multiple environments and in culture (Hmelo et al ; Rouco et al ; Frischkorn et al ; Lee et al ) and biologically relevant concentrations of AHLs have been found in Trichodesmium colonies (Van Mooy et al ). Taken together, it is likely that the microbiome could ubiquitously influence Trichodesmium N 2 fixation via quorum sensing pathways.…”

N2 fixation in free‐floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments

“…Consequently, we suggest that previous observations of higher or similar N 2 fixation rates in colonies compared with free‐floating trichomes in the field (Saino & Hattori, ; Letelier & Karl, ) were not due to O 2 microenvironments, but due to other factors not included in our laboratory setting. These might include positive effects of colony formation on the nutritional status of Trichodesmium that are manifested only under nutrient‐limited conditions in the field, such as enhanced dust dissolution (Rubin et al ., ) and more efficient interaction with bacterial associates producing siderophores and/or alkaline phosphatase (Chappell & Webb, ; Orcutt et al ., ; Lee et al ., ). By excluding these additional factors in our laboratory study under nutrient‐replete conditions, we revealed that O 2 microenvironments per se did not lead to higher N 2 fixation rates in colonies compared with free‐floating trichomes.…”