skip to main content


Title: Microbial and nutrient dynamics in mangrove, reef, and seagrass waters over tidal and diurnal time scales
In coral reefs and adjacent seagrass meadow and mangrove environments, short temporal scales (i.e. tidal, diurnal) may have important influences on ecosystem processes and community structure, but these scales are rarely investigated. This study examines how tidal and diurnal forcings influence pelagic microorganisms and nutrient dynamics in 3 important and adjacent coastal biomes: mangroves, coral reefs, and seagrass meadows. We sampled for microbial ( Bacteria and Archaea ) community composition, cell abundances and environmental parameters at 9 coastal sites on St. John, US Virgin Islands that spanned 4 km in distance (4 coral reefs, 2 seagrass meadows and 3 mangrove locations within 2 larger bays). Eight samplings occurred over a 48 h period, capturing day and night microbial dynamics over 2 tidal cycles. The seagrass and reef biomes exhibited relatively consistent environmental conditions and microbial community structure but were dominated by shifts in picocyanobacterial abundances that were most likely attributed to diel dynamics. In contrast, mangrove ecosystems exhibited substantial daily shifts in environmental parameters, heterotrophic cell abundances and microbial community structure that were consistent with the tidal cycle. Differential abundance analysis of mangrove-associated microorganisms revealed enrichment of pelagic oligotrophic taxa during high tide and enrichment of putative sediment-associated microbes during low tide. Our study underpins the importance of tidal and diurnal time scales in structuring coastal microbial and nutrient dynamics, with diel and tidal cycles contributing to a highly dynamic microbial environment in mangroves, and time of day likely contributing to microbial dynamics in seagrass and reef biomes.  more » « less
Award ID(s):
1736288 1536782
NSF-PAR ID:
10198821
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Aquatic Microbial Ecology
Volume:
85
ISSN:
0948-3055
Page Range / eLocation ID:
101 to 119
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Abstract. Mangrove forests are ecosystems that constitute a large portion of the world's coastline and span tidal zones below, between, and above thewaterline, and the ecosystem as a whole is defined by the health of these tidal microhabitats. However, we are only beginning to understand tidal-zone microbial biodiversity and the role of these microbiomes in nutrient cycling. While extensive research has characterized microbiomes inpristine vs. anthropogenically impacted mangroves, these have, largely, overlooked differences in tidal microhabitats (sublittoral, intertidal, andsupralittoral). Unfortunately, the small number of studies that have sought to characterize mangrove tidal zones have occurred in impacted biomes,making interpretation of the results difficult. Here, we characterized prokaryotic populations and their involvement in nutrient cycling across thetidal zones of a pristine mangrove within a Brazilian Environmental Protection Area of the Atlantic Forest. We hypothesized that the tidal zones inpristine mangroves are distinct microhabitats, which we defined as distinct regions that present spatial variations in the water regime and otherenvironmental factors, and as such, these are composed of different prokaryotic communities with distinct functional profiles. Samples werecollected in triplicate from zones below, between, and above the tidal waterline. Using 16S ribosomal RNA (rRNA) gene amplicon sequencing, we found distinctprokaryotic communities with significantly diverse nutrient-cycling functions, as well as specific taxa with varying contributions to functionalabundances between zones. Where previous research from anthropogenically impacted mangroves found the intertidal zone to have high prokaryoticdiversity and be functionally enriched in nitrogen cycling, we find that the intertidal zone from pristine mangroves has the lowest diversity and nofunctional enrichment, relative to the other tidal zones. The main bacterial phyla in all samples were Firmicutes, Proteobacteria,and Chloroflexi while the main archaeal phyla were Crenarchaeota and Thaumarchaeota. Our results differ slightly fromother studies where Proteobacteria is the main phyla in mangrove sediments and Firmicutes makes up only a small percentage ofthe communities. Salinity and organic matter were the most relevant environmental factors influencing these communities. Bacillaceae wasthe most abundant family at each tidal zone and showed potential to drive a large proportion of the cycling of carbon, nitrogen, phosphorus, andsulfur. Our findings suggest that some aspects of mangrove tidal zonation may be compromised by human activity, especially in the intertidal zone. 
    more » « less
  2. Johnson, Karyn N. (Ed.)
    ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down. 
    more » « less
  3. Tropical environments with unique abiotic and biotic factors—such as salt ponds, mangroves, and coral reefs—are often in close proximity. The heterogeneity of these environments is reflected in community shifts over short distances, resulting in high biodiversity. While phytoplankton assemblages physically associated with corals, particularly their symbionts, are well studied, less is known about phytoplankton diversity across tropical aquatic environments. We assess shifts in phytoplankton community composition along inshore to offshore gradients by sequencing and analyzing 16S rRNA gene amplicons using primers targeting the V1-V2 region that capture plastids from eukaryotic phytoplankton and cyanobacteria, as well as heterotrophic bacteria. Microbial alpha diversity computed from 16S V1-V2 amplicon sequence variant (ASV) data from 282 samples collected in and around Curaçao, in the Southern Caribbean Sea, varied more within the dynamic salt ponds, salterns, and mangroves, compared to the seemingly stable above-reef, off-reef, and open sea environments. Among eukaryotic phytoplankton, stramenopiles often exhibited the highest relative abundances in mangrove, above-reef, off-reef, and open sea environments, where cyanobacteria also showed high relative abundances. Within stramenopiles, diatom amplicons dominated in salt ponds and mangroves, while dictyochophytes and pelagophytes prevailed above reefs and offshore. Green algae and cryptophytes were also present, and the former exhibited transitions following the gradient from inland to offshore. Chlorophytes and prasinophyte Class IV dominated in salt ponds, while prasinophyte Class II, including Micromonas commoda and Ostreococcus Clade OII, had the highest relative abundances of green algae in mangroves, above-reef, off-reef, and the open sea. To improve Class II prasinophyte classification, we sequenced 18S rRNA gene amplicons from the V4 region in 41 samples which were used to interrelate plastid-based results with information on uncultured prasinophyte species from prior 18S rRNA gene-based studies. This highlighted the presence of newly described Ostreococcus bengalensis and two Micromonas candidate species. Network analyses identified co-occurrence patterns between individual phytoplankton groups, including cyanobacteria, and heterotrophic bacteria. Our study reveals multiple uncultured and novel lineages within green algae and dictyochophytes in tropical marine habitats. Collectively, the algal diversity patterns and potential co-occurrence relationships observed in connection to physicochemical and spatial influences help provide a baseline against which future change can be assessed. 
    more » « less
  4. Microorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km 2 . On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (>85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features. 
    more » « less
  5. Coral reef ecosystems are incredibly diverse marine biomes that rely on nutrient cycling by microorganisms to sustain high productivity in generally oligotrophic regions of the ocean. Understanding the composition of extracellular reef metabolites in seawater, the small organic molecules that serve as the currency for microorganisms, may provide insight into benthic-pelagic coupling as well as the complexity of nutrient cycling in coral reef ecosystems. Jardines de la Reina (JR), Cuba is an ideal environment to examine extracellular metabolites across protected and high-quality reefs. Here, we used liquid chromatography mass spectrometry (LC-MS) to quantify specific known metabolites of interest (targeted metabolomics approach) and to survey trends in metabolite feature composition (untargeted metabolomics approach) from surface and reef depth (6 – 14 m) seawater overlying nine forereef sites in JR. We found that untargeted metabolite feature composition was surprisingly similar between reef depth and surface seawater, corresponding with other biogeochemical and physicochemical measurements and suggesting that environmental conditions were largely homogenous across forereefs within JR. Additionally, we quantified 32 of 53 detected metabolites using the targeted approach, including amino acids, nucleosides, vitamins, and other metabolic intermediates. Two of the quantified metabolites, riboflavin and xanthosine, displayed interesting trends by depth. Riboflavin concentrations were higher in reef depth compared to surface seawater, suggesting that riboflavin may be produced by reef organisms at depth and degraded in the surface through photochemical oxidation. Xanthosine concentrations were significantly higher in surface reef seawater. 5′-methylthioadenosine (MTA) concentrations increased significantly within the central region of the archipelago, displaying biogeographic patterns that warrant further investigation. Here we lay the groundwork for future investigations of variations in metabolite composition across reefs, sources and sinks of reef metabolites, and changes in metabolites over environmental, temporal, and reef health gradients. 
    more » « less