Environmental Shaping of Sponge Associated Archaeal Communities

Turque, Aline S.; Batista, Daniela; Silveira, Cynthia B.; Cardoso, Alexander Machado; Vieira, Ricardo P.; Moraes, Fernando C.; Clementino, Maysa M.; Albano, Rodolpho Mattos; Paranhos, Rodolfo; Martins, Orlando B.; Muricy, Guilherme

doi:10.1371/journal.pone.0015774

Cited by 81 publications

(65 citation statements)

References 47 publications

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“…Individual Petrosia ficiformis sponges growing in well-illuminated habitats harbor cyanobacterial symbionts, while those growing in shaded areas, including caves, do not (21). A study near a highly polluted estuary in Brazil noted that nutrient concentrations played a role in the structuring of the different archaeal communities of conspecific sponges (23). In another study, experimental warming induced changes in the microbial community structure of Rhopaloeides odorabile (24).…”

mentioning

confidence: 99%

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

Weigel

Erwin

2016

Appl Environ Microbiol

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Sponges host diverse and complex communities of microbial symbionts that display a high degree of host specificity. The microbiomes of conspecific sponges are relatively constant, even across distant locations, yet few studies have directly examined the influence of abiotic factors on intraspecific variation in sponge microbial community structure. The contrast between intertidal and subtidal environments is an ideal system to assess the effect of environmental variation on sponge-microbe symbioses, producing two drastically different environments on a small spatial scale. Here, we characterized the microbial communities of individual intertidal and subtidal Hymeniacidon heliophila sponges, ambient seawater, and sediment from a North Carolina oyster reef habitat by partial (Illumina sequencing) and nearly full-length (clone libraries) 16S rRNA gene sequence analyses. Clone library sequences were compared to H. heliophila symbiont communities from the Gulf of Mexico and Brazil, revealing strong host specificity of dominant symbiont taxa across expansive geographic distances. Sediment and seawater samples yielded clearly distinct microbial communities from those found in H. heliophila. Despite the close proximity of the sponges sampled, significant differences between subtidal and intertidal sponges in the diversity, structure, and composition of their microbial communities were detected. Differences were driven by changes in the relative abundance of a few dominant microbial symbiont taxa, as well as the presence or absence of numerous rare microbial taxa. These findings suggest that extreme abiotic fluctuations, such as periodic air exposure in intertidal habitats, can drive intraspecific differences in complex host-microbe symbioses. Sponges form ancient symbioses (as described in reference 1) with a great diversity of bacterial, archaeal, and eukaryotic microorganisms (1, 2). Most of these microbial symbionts elude cultivation (3); thus, culture-independent techniques such as next-generation DNA sequencing are necessary to elucidate the immense diversity of microbial communities in marine sponges. For example, the sponge Rhopaloeides odorabile hosts nearly 3,000 unique microbial taxa (4). Symbiotic microbes can constitute up to 40% of the sponge mesohyl volume (5) and perform a variety of ecological functions in the host sponge (6). Sponge-associated microbial symbionts may play roles in the nutrient acquisition, chemical defense production, antifouling activity, and disease susceptibility of host sponges (1, 7). Despite the ubiquity of microbial symbionts in sponges, much is still unknown about their structure and ecological function.Sponges host microbial communities that are distinct from those found in seawater and exhibit a high degree of host specificity (4, 8, 9), even between closely related sponge species (10). Determining what structures these symbiotic communities is a current research priority, because it will provide insight into the maintenance of one of the most ancient metazoan-microbial symbio...

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mentioning

confidence: 99%

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

Weigel

Erwin

2016

Appl Environ Microbiol

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“…Archaeal amoA sequences were distinct from those found in other sponges (Bayer et al 2008, Meyer & Kuever 2008, Steger et al 2008, Hoffmann et al 2009, López-Legentil et al 2010, Turque et al 2010, Liu et al 2011, Han et al 2012, Radax et al 2012, Ribes et al 2012. The closest relative to sequences retrieved from the tropical sponge H. caerulea was from the coral Diploria strigosa (Beman et al 2007), while amoA se quences from water surrounding the sponge were similar to sequences retrieved from the warmwater sponge Siphonochalina sp.…”

Section: Diversity Of Sponge-associated Aoa and Aobmentioning

confidence: 83%

“…corticata and se quences from other sponge species (Meyer & Kuever 2008) supports the existence of sponge-specific clusters and vertically acquired Archaea within sponges. The existence of sponge-specific associated Archaea has also been suggested for other sponge species (Preston et al 1996, Holmes & Blanch 2007, Bayer et al 2008, Hoffmann et al 2009, Turque et al 2010, Radax et al 2012.…”

Section: Diversity Of Sponge-associated Aoa and Aobmentioning

confidence: 88%

“…Ammonia-oxidizing Archaea (AOA) have also been receiving increasing attention since the discovery of the ammonia-oxidizing thaumarchaeote Cenarchaeum symbiosum associated with the sponge Axinella mexicana (Preston et al 1996). Thaumarchaeotes, in particular, appear capable of oxidizing ammonia (Bayer et al 2008, Turque et al 2010, Liu et al 2011, Pester et al 2011. Recently, the presence of AOB and AOA was described for a diverse range of sponges from the Pacific, Caribbean, Mediterranean and North At lantic (Bayer et al 2008, Meyer & Kuever 2008, Steger et al 2008, López-Legentil et al 2010, Mohamed et al 2010, Liu et al 2011, Radax et al 2012.…”

Section: Introductionmentioning

confidence: 99%

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Diversity and abundance of ammonia-oxidizing Archaea and Bacteria in tropical and cold-water coral reef sponges

Cardoso¹,

Bleijswijk²,

Witte³

et al. 2013

Aquat. Microb. Ecol.

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We analysed the diversity and abundance of ammonia-oxidizing Archaea (AOA) and Bacteria (AOB) in the shallow warm-water sponge Halisarca caerulea and the deep cold-water sponges Higginsia thielei and Nodastrella nodastrella. The abundance of AOA and AOB was analysed using catalyzed reporter deposition-fluorescence in situ hybridization and (real-time) quantitative PCR (Q-PCR) targeting archaeal and bacterial amoA genes. Archaeal abundance was similar between sponge species, while bacterial abundance was higher in H. caerulea than in N. nodastrella and H. thielei. Q-PCR showed that AOA outnumbered AOB by a factor of 2 to 35, suggesting a larger role of AOA than of AOB in ammonia oxidation in sponges. PCR-denaturing gradient gel electrophoresis was performed to analyse the taxonomic affiliation of the microbial community associated with these sponges. Archaeal and bacterial amoA genes were found in all 3 sponges. The structure of the phylogenetic trees in relation to temperature and sponge species was analysed using all published amoA sequences retrieved from sponges. Temperature was an important factor influencing the distribution of nitrifiers in sponges. Both archaeal and bacterial amoA sponge sequences tended to cluster with sequences retrieved from habitats of similar temperature. This is the first time that similarity in AOB diversity is described between distantly related species (H. thielei belonging to the class Demospongiae, and N. nodastrella to Hexactinellida). The results described here support the idea of a relatively uniform microbial community between distantly related sponges and suggest that temperature (rather than phylogenetic distance) is determining the diversity of AOA and AOB in sponges.

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“…Archaeal communities have been found in sediments and in the anoxic zone of the water column (depth of 40 m) in the Tucuruí Reservoir (Graças et al, 2011). Archaea has also been found in seawater Cury et al, 2011;Francis et al, 2005), marine sediments (Bowman & McCuaig, 2003;Nakayama et al, 2011), wetlands (Sims et al, 2012) and in association with other organisms, such as sponges (Turque et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Distribution of Archaeal and Bacterial communities in a subtropical reservoir

et al. 2015

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Aim: Microbial communities play a central role in environmental process such as organic matter mineralization and the nutrient cycling process in aquatic ecosystems. Despite their ecological importance, variability of the structure of archaeal and bacterial communities in freshwater remains understudied. Methods: In the present study we investigated the richness and density of archaea and bacteria in the water column and sediments of the Itupararanga Reservoir. We also evaluated the relationship between the communities and the biotic and abiotic characteristics. Samples were taken at five depths in the water column next to the dam and three depths next to the reservoir entrance. Results: PCR-DGGE evaluation of the archaeal and bacterial communities showed that both were present in the water column, even in oxygenated conditions. Conclusions: The density of the bacteria (qPCR) was greater than that of the archaea, a result of the higher metabolic plasticity of bacteria compared with archaea.Keywords: freshwater; microbial communities; PCR/DGGE; real time PCR.Resumo: Objetivo: As comunidades microbianas desempenham papel crucial nos processos ambientais como na mineralização de matéria orgânica e ciclagem de nutrientes em ambientes aquáticos. No entanto, apesar da importância ecológica de archaea e bactéria em ambientes aquáticos, a estrutura destas comunidades permanece pouco estudada. Métodos: Neste sentido, nos avaliamos a riqueza e densidade de archaea e bactéria na coluna d'água e no sedimento do reservatório de Itupararanga e avaliamos as relações entre os fatores bióticos e abióticos. Para tanto, amostragens foram realizadas em cinco profundidades na região próxima a barragem e em três profundidades no ponto da entrada. Resultados: A partir de PCR-DGGE observou-se que ambas as comunidades distribuíram-se ao logo dos pontos de amostragem, mesmo em condições com presença de oxigênio. Conclusões: A densidade bacterianas, avaliada por qPCR foi maior do que a de archaea, provavelmente devido a maior plasticidade metabólica desses microrganismos.Palavras-chave: águas continentais; comunidade microbiana; PCR/DGGE; real time PCR. Acta Limnologica Brasiliensia

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Environmental Shaping of Sponge Associated Archaeal Communities

Cited by 81 publications

References 47 publications

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

Diversity and abundance of ammonia-oxidizing Archaea and Bacteria in tropical and cold-water coral reef sponges

Distribution of Archaeal and Bacterial communities in a subtropical reservoir

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