Global-scale structure of the eelgrass microbiome

Abstract

Plant-associated microorganisms are essential for their hosts' survival and performance. Yet, most plant microbiome studies to date have focused on terrestrial species sampled across relatively small spatial scales. Here, we report the results of a global-scale analysis of microbial communities associated with leaf and root surfaces of the marine eelgrass Zostera marina throughout its range in the Northern Hemisphere. By contrasting host microbiomes with those of surrounding seawater and sediment, we uncovered the structure, composition, and variability of microbial communities associated with eelgrass. We also investigated hypotheses about the assembly of the eelgrass microbiome using a metabolic modeling approach. Our results reveal leaf communities displaying high variability and spatial turnover that mirror their adjacent coastal seawater microbiomes. By contrast, roots showed relatively low compositional turnover and were distinct from surrounding sediment communities, a result driven by the enrichment of predicted sulfur-oxidizing bacterial taxa on root surfaces. Predictions from metabolic modeling of enriched taxa were consistent with a habitat-filtering community assembly mechanism whereby similarity in resource use drives taxonomic cooccurrence patterns on belowground, but not aboveground, host tissues. Our work provides evidence for a core eelgrass root microbiome with putative functional roles and highlights potentially disparate processes influencing microbial community assembly on different plant compartments.IMPORTANCE Plants depend critically on their associated microbiome, yet the structure of microbial communities found on marine plants remains poorly understood in comparison to that for terrestrial species. Seagrasses are the only flowering plants that live entirely in marine environments. The return of terrestrial seagrass ancestors to oceans is among the most extreme habitat shifts documented in plants, making them an ideal testbed for the study of microbial symbioses with plants that experience relatively harsh abiotic conditions. In this study, we report the results of a global sampling effort to extensively characterize the structure of microbial communities associated with the widespread seagrass species Zostera marina, or eelgrass, across its geographic range. Our results reveal major differences in the structure and composition of above-versus belowground microbial communities on eelgrass surfaces, as well as their relationships with the environment and host.

Sympatric kelp species share a large portion of their surface bacterial communities

“…Yet, data from wild populations of great apes show that the magnitude of species‐specific differences in microbial structure is reduced when hosts occur in sympatry (Moeller et al ., ), suggesting that the environment plays an important role in determining the composition of host‐associated communities. The homogenizing effect of colonization by environmental bacteria is especially strong for microbial communities associated with the external surfaces of their hosts (Song et al ., ; Lemieux‐Labonte et al ., ), including marine organisms, whose surfaces are constantly in contact with the rich diversity of ambient free‐living marine microbes (Fahimipour et al ., ).…”

Seagrass rhizosphere microenvironment alters plant‐associated microbial community composition

“…The microbial community composition in the artificial sediment was similar to that reported from other seagrass‐vegetated natural sediments (e.g., Jensen et al ., ; Cúcio et al ., ); with many members of the rhizospheric microbial community affiliated with the sulphur cycle (Cúcio et al ., ; Ettinger et al ., ; Fahimipour et al ., ). Compared to the bulk sediment, we observed higher mean relative abundance of SRB taxa including OTUs matching Desulfovibrio sp., especially around the root apical meristems, where members of the SRB class Clostridia (Devereux, ; Sallam and Steinbüchel, ) dominated, with ∼ 57% of sequences affiliated with this bacterial class ( t (5) RAM‐BS = 4.015, p = 0.01; t (4) RAM‐NC = 16.944, p < 0.001; Fig.…”

“…Seagrass meadows are high‐value ecosystems (Costanza et al ., ) that provide numerous ecosystem services to marine environments, such as facilitating nursery areas for many juvenile fish and crustaceans (Harborne et al ., ; Larkum et al ., ), improving water quality through increased sedimentation (Ward et al ., ; Madsen et al ., ), providing a main food source for iconic marine animals such as sea turtles and dugongs, and by having a high ability to sequester carbon in the sediment (Duarte et al ., ; Fourqurean et al ., ). Seagrass ecosystems harbour a unique microbiome including populations of microbes attached to seagrass leaves and within the rhizosphere, with microorganisms involved in the sulphur cycle known to play particularly important functional roles (e.g., Devereux, ; Jensen et al ., ; Cúcio et al ., ; Fahimipour et al ., ). However, a quantitative understanding of the importance of this microbiome on the fitness of seagrass plants is lacking (York et al ., ).…”

“…Seagrass‐driven modulation of the rhizosphere microhabitat has been suggested to initiate mutualistic relationships between seagrasses and diazotrophic SRB based on reciprocal nutrient exchange, whereby the seagrass host provides a carbon source to the diazotrophs that in return fix dinitrogen (Hansen et al ., ; Welsh et al ., ; Nielsen et al ., ). Sulphide‐oxidizing bacteria within oxic microenvironments in the rhizosphere have also been proposed to play an important role in sediment detoxification (Jensen et al ., ; Cúcio et al ., ; Fahimipour et al ., ). Bacterial‐mediated H 2 S oxidation is 10 4 –10 5 times faster than spontaneous chemical oxidation (Jørgensen and Revsbech, ; Nelson et al ., ) and given ample O 2 supply, SOB may thus efficiently remove toxic H 2 S, facilitating seagrass colonization of highly sulfidic sediments.…”

Discovery of a novel potexvirus in the seagrass Thalassia testudinum from Tampa Bay, Florida

“…Recently, there has been a growing appreciation of the importance of microbial communities living in and on seagrasses, referred to as the seagrass microbiome (Bengtsson et al ; Ettinger et al ; Fahimipour et al ; Ugarelli et al ). Microbiomes, which include all microbes (archaea, bacteria, fungi, protists, and viruses) associated with a given organism, are key determinants of a plant's health and productivity by influencing processes such as nutrient uptake and immunity or by driving the evolution of the host (Turner et al ; Rosenberg and Zilber‐Rosenberg ).…”