Title: Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles
ABSTRACT Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describe the gut microbiomes of two hadal snailfishes, Pseudoliparis swirei (Mariana Trench) and Notoliparis kermadecensis (Kermadec Trench), using 16S rRNA gene amplicon sequencing. We contextualize these microbiomes with comparisons to the abyssal macrourid Coryphaenoides yaquinae and the continental shelf-dwelling snailfish Careproctus melanurus . The microbial communities of the hadal snailfishes were distinct from their shallower counterparts and were dominated by the same sequences related to the Mycoplasmataceae and Desulfovibrionaceae . These shared taxa indicate that symbiont lineages have remained similar to the ancestral symbiont since their geographic separation or that they are dispersed between geographically distant trenches and subsequently colonize specific hosts. The abyssal and hadal fishes contained sequences related to known, cultured piezophiles, microbes that grow optimally under high hydrostatic pressure, including Psychromonas , Moritella , and Shewanella . These taxa are adept at colonizing nutrient-rich environments present in the deep ocean, such as on particles and in the guts of hosts, and we hypothesize they could make a dietary contribution to deep-sea fishes by degrading chitin and producing fatty acids. We characterize the gut microbiota within some of the deepest fishes to provide new insight into the diversity and distribution of host-associated microbial taxa and the potential of these animals, and the microbes they harbor, for understanding adaptation to deep-sea habitats. IMPORTANCE Hadal trenches, characterized by high hydrostatic pressures and low temperatures, are one of the most extreme environments on our planet. By examining the microbiome of abyssal and hadal fishes, we provide insight into the diversity and distribution of host-associated life at great depth. Our findings show that there are similar microbial populations in fishes geographically separated by thousands of miles, reflecting strong selection for specific microbial lineages. Only a few psychropiezophilic taxa, which do not reflect the diversity of microbial life at great depth, have been successfully isolated in the laboratory. Our examination of deep-sea fish microbiomes shows that typical high-pressure culturing methodologies, which have largely remained unchanged since the pioneering work of Claude ZoBell in the 1950s, may simulate the chemical environment found in animal guts and helps explain why the same deep-sea genera are consistently isolated. more »« less
Abstract The deepest part of the global ocean, hadal trenches, are considered to act as depocenters for organic material. Relatively high microbial activity has been demonstrated in the deepest sections of some hadal trenches, but the deposition dynamics are thought to be spatially and temporally variable. Here, we explore sediment characteristics and in-situ benthic oxygen uptake along two trenches with contrasting surface primary productivity: the Kermadec and Atacama trenches. We find that benthic oxygen consumption varies by a factor of about 10 between hadal sites but is in all cases intensified relative to adjacent abyssal plains. The benthic oxygen uptake of the two trench regions reflects the difference in surface production, whereas variations within each trench are modulated by local deposition dynamics. Respiratory activity correlates with the sedimentary inventories of organic carbon and phytodetrital material. We argue that hadal trenches represent deep sea hotspots for early diagenesis and are more diverse and dynamic environments than previously recognized.
Rojas, Connie A.; Holekamp, Kay E.; Viladomat Jasso, Mariette; Souza, Valeria; Eisen, Jonathan A.; Theis, Kevin R.(
, mSystems)
Hird, Sarah M.
(Ed.)
The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specific and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas’ guts; some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species-level matches to genomes in existing reference databases. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores, and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores, but over 80% of MAGs were novel and from species not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis.
Dysbiosis of coral microbiomes results from various biotic and environmental stressors, including interactions with important reef fishes which may act as vectors of opportunistic microbes via deposition of fecal material. Additionally, elevated sea surface temperatures have direct effects on coral microbiomes by promoting growth and virulence of opportunists and putative pathogens, thereby altering host immunity and health. However, interactions between these biotic and abiotic factors have yet to be evaluated. Here, we used a factorial experiment to investigate the combined effects of fecal pellet deposition by the widely distributed surgeonfish Ctenochaetus striatus and elevated sea surface temperatures on microbiomes associated with the reef-building coral Porites lobata . Our results showed that regardless of temperature, exposure of P. lobata to C. striatus feces increased alpha diversity, dispersion, and lead to a shift in microbial community composition – all indicative of microbial dysbiosis. Although elevated temperature did not result in significant changes in alpha and beta diversity, we noted an increasing number of differentially abundant taxa in corals exposed to both feces and thermal stress within the first 48h of the experiment. These included opportunistic microbial lineages and taxa closely related to potential coral pathogens (i.e., Vibrio vulnificus , Photobacterium rosenbergii ). Some of these taxa were absent in controls but present in surgeonfish feces under both temperature regimes, suggesting mechanisms of microbial transmission and/or enrichment from fish feces to corals. Importantly, the impact to coral microbiomes by fish feces under higher temperatures appeared to inhibit wound healing in corals, as percentages of tissue recovery at the site of feces deposition were lower at 30°C compared to 26°C. Lower percentages of tissue recovery were associated with greater relative abundance of several bacterial lineages, with some of them found in surgeonfish feces (i.e., Rhodobacteraceae, Bdellovibrionaceae, Crocinitomicaceae). Our findings suggest that fish feces interact with elevated sea surface temperatures to favor microbial opportunism and enhance dysbiosis susceptibility in P. lobata . As the frequency and duration of thermal stress related events increase, the ability of coral microbiomes to recover from biotic stressors such as deposition of fish feces may be greatly affected, ultimately compromising coral health and resilience.
Blum, Joel D.; Drazen, Jeffrey C.; Johnson, Marcus W.; Popp, Brian N.; Motta, Laura C.; Jamieson, Alan J.(
, Proceedings of the National Academy of Sciences)
Mercury isotopic compositions of amphipods and snailfish from deep-sea trenches reveal information on the sources and transformations of mercury in the deep oceans. Evidence for methyl-mercury subjected to photochemical degradation in the photic zone is provided by odd-mass independent isotope values (Δ199Hg) in amphipods from the Kermadec Trench, which average 1.57‰ (±0.14,n= 12, SD), and amphipods from the Mariana Trench, which average 1.49‰ (±0.28,n= 13). These values are close to the average value of 1.48‰ (±0.34,n= 10) for methyl-mercury in fish that feed at ∼500-m depth in the central Pacific Ocean. Evidence for variable contributions of mercury from rainfall is provided by even-mass independent isotope values (Δ200Hg) in amphipods that average 0.03‰ (±0.02,n= 12) for the Kermadec and 0.07‰ (±0.01,n= 13) for the Mariana Trench compared to the rainfall average of 0.13 (±0.05,n= 8) in the central Pacific. Mass-dependent isotope values (δ202Hg) are elevated in amphipods from the Kermadec Trench (0.91 ±0.22‰,n= 12) compared to the Mariana Trench (0.26 ±0.23‰,n= 13), suggesting a higher level of microbial demethylation of the methyl-mercury pool before incorporation into the base of the foodweb. Our study suggests that mercury in the marine foodweb at ∼500 m, which is predominantly anthropogenic, is transported to deep-sea trenches primarily in carrion, and then incorporated into hadal (6,000-11,000-m) food webs. Anthropogenic Hg added to the surface ocean is, therefore, expected to be rapidly transported to the deepest reaches of the oceans.
Abstract. Elevated organic matter (OM) concentrations are found in hadalsurface sediments relative to the surrounding abyssal seabed. However, theorigin of this biological material remains elusive. Here, we report on thecomposition and distribution of cellular membrane intact polar lipids (IPLs)extracted from surface sediments around the deepest points of the AtacamaTrench and adjacent bathyal margin to assess and constrain the sources oflabile OM in the hadal seabed. Multiscale bootstrap resampling of IPLs'structural diversity and abundance indicates distinct lipid signatures inthe sediments of the Atacama Trench that are more closely related to thosefound in bathyal sediments than to those previously reported for the upperocean water column in the region. Whereas the overall number of unique IPLstructures in hadal sediments contributes a small fraction of the total IPLpool, we also report a high contribution of phospholipids with mono- anddi-unsaturated fatty acids that are not associated with photoautotrophicsources and that resemble traits of physiological adaptation to highpressure and low temperature. Our results indicate that IPLs in hadalsediments of the Atacama Trench predominantly derive from in situ microbialproduction and biomass, whereas the export of the most labile lipidcomponent of the OM pool from the euphotic zone and the overlying oxygenminimum zone is neglectable. While other OM sources such as the downslopeand/or lateral transport of labile OM cannot be ruled out and remain to bestudied, they are likely less important in view of the lability ofester-bond IPLs. Our results contribute to the understanding of themechanisms that control the delivery of labile OM to this extreme deep-seaecosystem. Furthermore, they provide insights into some potentialphysiological adaptation of the in situ microbial community to high pressure andlow temperature through lipid remodeling.
Blanton, Jessica M., Peoples, Logan M., Gerringer, Mackenzie E., Iacuaniello, Caroline M., Gallo, Natalya D., Linley, Thomas D., Jamieson, Alan J., Drazen, Jeffrey C., Bartlett, Douglas H., and Allen, Eric E. Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles. Retrieved from https://par.nsf.gov/biblio/10343204. mSphere 7.2 Web. doi:10.1128/msphere.00032-22.
Blanton, Jessica M., Peoples, Logan M., Gerringer, Mackenzie E., Iacuaniello, Caroline M., Gallo, Natalya D., Linley, Thomas D., Jamieson, Alan J., Drazen, Jeffrey C., Bartlett, Douglas H., & Allen, Eric E. Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles. mSphere, 7 (2). Retrieved from https://par.nsf.gov/biblio/10343204. https://doi.org/10.1128/msphere.00032-22
Blanton, Jessica M., Peoples, Logan M., Gerringer, Mackenzie E., Iacuaniello, Caroline M., Gallo, Natalya D., Linley, Thomas D., Jamieson, Alan J., Drazen, Jeffrey C., Bartlett, Douglas H., and Allen, Eric E.
"Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles". mSphere 7 (2). Country unknown/Code not available. https://doi.org/10.1128/msphere.00032-22.https://par.nsf.gov/biblio/10343204.
@article{osti_10343204,
place = {Country unknown/Code not available},
title = {Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles},
url = {https://par.nsf.gov/biblio/10343204},
DOI = {10.1128/msphere.00032-22},
abstractNote = {ABSTRACT Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describe the gut microbiomes of two hadal snailfishes, Pseudoliparis swirei (Mariana Trench) and Notoliparis kermadecensis (Kermadec Trench), using 16S rRNA gene amplicon sequencing. We contextualize these microbiomes with comparisons to the abyssal macrourid Coryphaenoides yaquinae and the continental shelf-dwelling snailfish Careproctus melanurus . The microbial communities of the hadal snailfishes were distinct from their shallower counterparts and were dominated by the same sequences related to the Mycoplasmataceae and Desulfovibrionaceae . These shared taxa indicate that symbiont lineages have remained similar to the ancestral symbiont since their geographic separation or that they are dispersed between geographically distant trenches and subsequently colonize specific hosts. The abyssal and hadal fishes contained sequences related to known, cultured piezophiles, microbes that grow optimally under high hydrostatic pressure, including Psychromonas , Moritella , and Shewanella . These taxa are adept at colonizing nutrient-rich environments present in the deep ocean, such as on particles and in the guts of hosts, and we hypothesize they could make a dietary contribution to deep-sea fishes by degrading chitin and producing fatty acids. We characterize the gut microbiota within some of the deepest fishes to provide new insight into the diversity and distribution of host-associated microbial taxa and the potential of these animals, and the microbes they harbor, for understanding adaptation to deep-sea habitats. IMPORTANCE Hadal trenches, characterized by high hydrostatic pressures and low temperatures, are one of the most extreme environments on our planet. By examining the microbiome of abyssal and hadal fishes, we provide insight into the diversity and distribution of host-associated life at great depth. Our findings show that there are similar microbial populations in fishes geographically separated by thousands of miles, reflecting strong selection for specific microbial lineages. Only a few psychropiezophilic taxa, which do not reflect the diversity of microbial life at great depth, have been successfully isolated in the laboratory. Our examination of deep-sea fish microbiomes shows that typical high-pressure culturing methodologies, which have largely remained unchanged since the pioneering work of Claude ZoBell in the 1950s, may simulate the chemical environment found in animal guts and helps explain why the same deep-sea genera are consistently isolated.},
journal = {mSphere},
volume = {7},
number = {2},
author = {Blanton, Jessica M. and Peoples, Logan M. and Gerringer, Mackenzie E. and Iacuaniello, Caroline M. and Gallo, Natalya D. and Linley, Thomas D. and Jamieson, Alan J. and Drazen, Jeffrey C. and Bartlett, Douglas H. and Allen, Eric E.},
editor = {Campbell, Barbara J.}
}
Warning: Leaving National Science Foundation Website
You are now leaving the National Science Foundation website to go to a non-government website.
Website:
NSF takes no responsibility for and exercises no control over the views expressed or the accuracy of
the information contained on this site. Also be aware that NSF's privacy policy does not apply to this site.
