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Diel population and functional synchrony of microbial communities on coral reefs.

ABSTRACT: On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs.

SUBMITTER: Kelly LW

PROVIDER: S-EPMC6461649 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Diel population and functional synchrony of microbial communities on coral reefs.

Kelly Linda Wegley LW Nelson Craig E CE Haas Andreas F AF Naliboff Douglas S DS Calhoun Sandi S Carlson Craig A CA Edwards Robert A RA Fox Michael D MD Hatay Mark M Johnson Maggie D MD Kelly Emily L A ELA Lim Yan Wei YW Macherla Saichetana S Quinlan Zachary A ZA Silva Genivaldo Gueiros Z GGZ Vermeij Mark J A MJA Zgliczynski Brian B Sandin Stuart A SA Smith Jennifer E JE Rohwer Forest F

Nature communications 20190412 1

On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is ...[more]

PMID: 30979882

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Project description:Reef organisms influence microorganisms within the surrounding seawater, yet the spatial and temporal dynamics of seawater microbial communities located in proximity to corals are rarely investigated. To better understand reef seawater microbial community dynamics over time and space, we collected small-volume seawater samples during the day and night over a 72 hour period from three locations that differed in spatial distance from 5 Porites astreoides coral colonies on a shallow reef in St. John, U.S. Virgin Islands: near-coral (sampled 5 cm horizontally from each colony), reef-depth (sampled 2 m above each colony) and surface seawater (sampled 1 m from the seawater surface). At all time points and locations, we quantified abundances of microbial cells, sequenced small subunit rRNA genes of bacterial and archaeal communities, and measured inorganic nutrient concentrations. Prochlorococcus and Synechococcus cells were consistently elevated at night compared to day and these abundances changed over time, corresponding with temperature, nitrite, and silicate concentrations. During the day, bacterial and archaeal alpha diversity was significantly higher in reef-depth and near-coral seawater compared to the surface seawater, signifying that the reef influences the diversity of the seawater microorganisms. At night, alpha diversity decreased across all samples, suggesting that photosynthesis may favor a more taxonomically diverse community. While Prochlorococcus exhibited consistent temporal rhythmicity, additional taxa were enriched in reef seawater at night compared to day or in reef-depth compared to surface seawater based on their normalized sequence counts. There were some significant differences in nutrient concentrations and cell abundances between reef-depth and near-coral seawater but no clear trends. This study demonstrates that temporal variation supersedes small-scale spatial variation in proximity to corals in reef seawater microbial communities. As coral reefs continue to change in benthic composition worldwide, monitoring microbial composition in response to temporal changes and environmental fluctuations will help discern normal variability from longer lasting changes attributed to anthropogenic stressors and global climate change.

Project description:The most important source of energy to tropical shallow water coral reefs is light, the transformation of which ultimately limits reef biomass and growth. Therefore, measurements of productivity (primary production, P) for benthic reef organisms and communities are critical to understand reef functioning. Short-term (minutes to hours) P measurements of reef photosynthesizers virtually always produce the classic hyperbolic tangent (or similar) P-E (irradiance) relationship, with P rapidly rising to a saturation point as E increases. Longer-term (days to weeks), larger-scale investigations of natural reef communities typically do not explore P-E relationships, but the few that do show no saturation of time-integrated P with high time-integrated E. In this paper we present a modeling study to reconcile this apparent contradiction. We used 52 published short-term (instantaneous) P-E curves of organisms (corals, algae) and communities (corals, mixed corals and algae) from different reefs in the Indo-Pacific and the Caribbean, each coupled with 928 diel light curves comprising a wide range of cloud cover scenarios. The diel light curves provided instantaneous E at 1-minute intervals, from which we calculated corresponding instantaneous P using the different published P-E relationships. We integrated both variables to calculate time-integrated E and P. Time-integrated E varied up to 18-fold due to changes in cloud cover and season. We found that, despite routine saturation of instantaneous P, day-scale P-E relationships were near linear in all cases, with slightly decreased linearity in cases where instantaneous light saturation occurred very early during the day. This indicates that the Functional Convergence Hypothesis (FCH) developed by terrestrial ecologists may also apply for reef photosynthesizers. The FCH states that despite short-term light saturation, plants on average do not absorb more light than they can use, since resource allocations are strictly coordinated and tailored towards an optimal use. Thus, there is no contradiction: At the growth time scale (? day), P should be expected to be a near linear function of E. One implication is that reef P can be estimated using rapid optical measurements, as opposed to traditional, laborious respirometry methods. The requirement going forward is to derive appropriate values for light-use efficiency, which is the rate at which the plant or community converts absorbed light into fixed carbon.

Dataset Information

Diel population and functional synchrony of microbial communities on coral reefs.

Publications

Diel population and functional synchrony of microbial communities on coral reefs.

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