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Mangroves are coastal environments that provide resources for adjacent ecosystems due to their high productivity, organic matter decomposition, and carbon cycling by microbial communities in sediments. Since the industrial revolution, the increase of Greenhouse Gases (GHG) released due to fossil fuel burning led to many environmental abnormalities such as an increase in average temperature and ocean acidification. Based on the hypothesis that climate change modifies the microbial diversity associated with decaying organic matter in mangrove sediments, this study aimed to evaluate the microbial diversity under simulated climate change conditions during the litter decomposition process and the emission of GHG. Thus, microcosms containing organic matter from the three main plant species found in mangroves throughout the State of São Paulo, Brazil (Rhizophora mangle, Laguncularia racemosa, and Avicennia schaueriana) were incubated simulating climate changes (increase in temperature and pH). The decay rate was higher in the first seven days of incubation, but the differences between the simulated treatments were minor. GHG fluxes were higher in the first ten days and higher in samples under increased temperature. The variation in time resulted in substantial impacts on α-diversity and community composition, initially with a greater abundance of Gammaproteobacteria for all plant species despite the climate conditions variations. The PCoA analysis reveals the chronological sequence in ß-diversity, indicating the increase of Deltaproteobacteria at the end of the process. The GHG emission varied in function of the organic matter source with an increase due to the elevated temperature, concurrent with the rise in the Deltaproteobacteria population. Thus, these results indicate that under the expected climate change scenario for the end of the century, the decomposition rate and GHG emissions will be potentially higher, leading to a harmful feedback loop of GHG production. This process can happen independently of an impact on the bacterial community structure due to these changes.

RESUMO

Leaf decomposition is the primary process in release of nutrients in the dynamic mangrove habitat, supporting the ecosystem food webs. On most environments, fungi are an essential part of this process. However, due to the peculiarities of mangrove forests, this group is currently neglected. Thus, this study tests the hypothesis that fungal communities display a specific succession pattern in different mangrove species and this due to differences in their ecological role. A molecular approach was employed to investigate the dynamics of the fungal community during the decomposition of three common plant species (Rhizophora mangle, Laguncularia racemosa, and Avicennia schaueriana) from a mangrove habitat located at the southeast of Brazil. Plant material was the primary driver of fungi communities, but time also was marginally significant for the process, and evident changes in the fungal community during the decomposition process were observed. The five most abundant classes common to all the three plant species were Saccharomycetes, Sordariomycetes, Tremellomycetes, Eurotiomycetes, and Dothideomycetes, all belonging to the Phylum Ascomycota. Microbotryomycetes class were shared only by A. schaueriana and L. racemosa, while Agaricomycetes class were shared by L. racemosa and R. mangle. The class Glomeromycetes were shared by A. schaueriana and R. mangle. The analysis of the core microbiome showed that Saccharomycetes was the most abundant class. In the variable community, Sordariomycetes was the most abundant one, mainly in the Laguncularia racemosa plant. The results presented in this work shows a specialization of the fungal community regarding plant material during litter decomposition which might be related to the different chemical composition and rate of degradation.

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Social interactions impact microbial communities and these relationships are mediated by small molecules. The chemical ecology of bacteria on the phylloplane environment is still little explored. The harsh environmental conditions found on leaf surface require high metabolic performances of the bacteria in order to survive. That is interesting both for scientific fields of prospecting natural molecules and for the ecological studies. Important queries about the bacterial lifestyle on leaf surface remain not fully comprehended. Does the hostility of the environment increase the populations' cellular altruism by the production of molecules, which can benefit the whole community? Or does the reverse occur and the production of molecules related to competition between species is increased? Does the phylogenetic distance between the bacterial populations influence the chemical profile during social interactions? Do phylogenetically related bacteria tend to cooperate more than the distant ones? The phylloplane contains high levels of yet uncultivated microorganisms, and understanding the molecular basis of the social networks on this habitat is crucial to gain new insights on the ecology of the mysterious community members due to interspecies molecular dependence. Here, we review and discuss what is known about bacterial social interactions and their chemical lifestyle on leaf surface.

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Mangroves are dynamic and unique ecosystems that provide important ecological services to coastal areas. The phylloplane is one of the greatest microbial habitats, and most of its microorganisms are uncultivated under common laboratory conditions. Bacterial community structure of Laguncularia racemosa phylloplane, a well-adapted mangrove species with salt exudation at foliar levels, was accessed through 16S rRNA amplicon sequencing. Sampling was performed in three different sites across a transect from upland to the seashore in a preserved mangrove forest located in the city of Cananéia, São Paulo State, Brazil. Higher bacterial diversity was observed in intermediary locations between the upland and the seashore, showing that significant intraspecific spatial variation in bacterial communities exists between a single host species with the selection of specific population between an environmental transect.

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BACKGROUND: Mangroves are important coastal ecosystems known for high photosynthetic productivity and the ability to support marine food chains through supply of dissolved carbon or particular organic matter. Most of the carbon found in mangroves is produced by its vegetation and is decomposed in root associated sediment. This process involves a tight interaction between microbial populations, litter chemical composition, and environmental parameters. Here, we study the complex interactions found during litter decomposition in mangroves by applying network analysis to metagenomic data. METHODS: Leaves of three species of mangrove trees typically found in the southeast of Brazil (Rhizophora mangle, Laguncularia racemosa, and Avicennia schaueriana) were collected in separate litter bags and left on three different mangroves for 60 days. These leaves were subsequently used for metagenome sequencing using Ion Torrent technology. Sequences were annotated in MG-RAST and used for network construction using MENAp. RESULTS: The most common phyla were Proteobacteria (classes Gamma and Alphaproteobacteria) followed by Firmicutes (Clostridia and Bacilli). The most abundant protein clusters were associated with the metabolism of carbohydrates, amino acids, and proteins. Non-metric multidimensional scaling of the metagenomic data indicated that substrate (i.e., tree species) did not significantly select for a specific community. Both networks exhibited scale-free characteristics and small world structure due to the low mean shortest path length and high average clustering coefficient. These networks also had a low number of hub nodes most of which were module hubs. DISCUSSION: This study demonstrates that under different environmental pressures (i.e., plant species or mangrove location) the microbial community associated with the decaying material forms a robust and stable network.

RESUMO

In this study, 16S rRNA gene amplicon sequencing was used to assess bacterial diversity and dynamics throughout different stages of leaves decomposition of three plant species (Rhizophora mangle, Laguncularia racemosa, and Avicennia schaueriana) in three distinct mangroves of São Paulo state, Brazil. The experiments were conducted in microcosms. Phylogenetic diversity (Faiths' PD) index showed differences between samples and suggested that some treatments like R. mangle increased their bacterial diversity through time. Principal coordinate analysis revealed that community's profile varied based on mangroves, followed by plant species and time. A clear succession patterns was observed in this study, i.e., some microorganisms with low abundance in the initial phases gradually became dominant (e.g., Alphaproteobacteria), whereas microbes that were initially predominant became low (e.g., Gammaproteobacteria). Co-occurrence analyses were performed for all times of plant degradation aiming to better understand the relationships between bacterial populations. The c-score index was done to test the randomness of the community assemblage during the stages of decomposition. For all degradation time points, the values of the observed c-score were higher than the values of the simulated c-score. This result indicated that during plant decomposition, the bacterial communities presented less co-occurrence than expected by chance and that these communities were not randomly assembled but instead they are driven by species interactions. Network analyses results showed that in the conditions presented in this experiment, the initial stages of leaf decomposition formed more connected and complex networks than the later stages. These results suggest that resource competition was a determinant in these specific mangroves during plant degradation, mainly in the initial periods.

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