Ultrastructural observations on prokaryotic associates of benthic foraminifera : food, mutualistic symbionts, or parasites?

© The Author(s), 2017. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Marine Micropaleontology 138 (2018): 33-45, doi:10.1016/j.marmicro.2017.09.001.Because prokaryotes (Eubacteria, Archaea) are ubiquitous in the marine realm, it may not be surprising that they are important to the diet of at least some foraminifera. Over recent decades, Transmission Electron Microscopy (TEM) has revealed that, at the ultrastructural level, additional intimate relationships exist between prokaryotes and foraminifera. For example, the cytoplasm of a variety of benthic foraminiferal species contains intact prokaryotes. Other benthic foraminiferal species support prokaryotic populations on their exterior. Some of these prokaryote-foraminifera associations are sufficiently consistent to be considered symbioses. Symbiotic relationships include beneficial associations (mutualism; commensalism) to detrimental associations (parasitism). Here, we provide a synopsis of known foraminiferal- prokaryotic symbioses and TEM micrographs illustrating many specific associations. We further comment on and illustrate additional interactions such as bacterial scavenging on foraminifera and foraminiferal feeding on prokaryotes. Documenting and understanding all of these microbial interactions will contribute to a more comprehensive knowledge of benthic marine ecology and biology.JMB’s contributions were funded by US NSF funding over many years, most recently NSF grant OCE-1634469, as well as the WHOI Robert W. Morse Chair for Excellence in Oceanography and The Investment in Science Fund at WHOI. MT and HN’s contributions were funded by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (no. 24340131 to MT and no. 22740340 to HN)

16S rRNA Gene Metabarcoding Indicates Species-Characteristic Microbiomes in Deep-Sea Benthic Foraminifera

Foraminifera are unicellular eukaryotes that are an integral part of benthic fauna in many marine ecosystems, including the deep sea, with direct impacts on benthic biogeochemical cycles. In these systems, different foraminiferal species are known to have a distinct vertical distribution, i.e., microhabitat preference, which is tightly linked to the physico-chemical zonation of the sediment. Hence, foraminifera are well-adapted to thrive in various conditions, even under anoxia. However, despite the ecological and biogeochemical significance of foraminifera, their ecology remains poorly understood. This is especially true in terms of the composition and diversity of their microbiome, although foraminifera are known to harbor diverse endobionts, which may have a significant meaning to each species' survival strategy. In this study, we used 16S rRNA gene metabarcoding to investigate the microbiomes of five different deep-sea benthic foraminiferal species representing differing microhabitat preferences. The microbiomes of these species were compared intra- and inter-specifically, as well as with the surrounding sediment bacterial community. Our analysis indicated that each species was characterized with a distinct, statistically different microbiome that also differed from the surrounding sediment community in terms of diversity and dominant bacterial groups. We were also able to distinguish specific bacterial groups that seemed to be strongly associated with particular foraminiferal species, such as the family Marinilabiliaceae for Chilostomella ovoidea and the family Hyphomicrobiaceae for Bulimina subornata and Bulimina striata. The presence of bacterial groups that are tightly associated to a certain foraminiferal species implies that there may exist unique, potentially symbiotic relationships between foraminifera and bacteria that have been previously overlooked. Furthermore, the foraminifera contained chloroplast reads originating from different sources, likely reflecting trophic preferences and ecological characteristics of the different species. This study demonstrates the potential of 16S rRNA gene metabarcoding in resolving the microbiome composition and diversity of eukaryotic unicellular organisms, providing unique in situ insights into enigmatic deep-sea ecosystems.Peer reviewe

Deep-sea freezer

Recovery of samples from the deep ocean in pristine condition is difficult due to large environmental differences between the deep and surface waters through which the samples necessarily must be transported. Here, we propose a concept for deep-sea sample recovery: a deep-sea freezer using thermoelectric cooling capable of generating ice in the deep and recover them frozen on-board ships. As a proof of concept, we present the DSF-α, a prototype Deep-Sea Freezer based on Peltier device rated at 2000 m. In situ assessments of the DSF-α on remotely operated vehicles showed its capacity to reach freezing (-13.0°C) temperatures in the deep, as well as recovering seawater frozen on deck. Although the DSF-α is limited in that achieving sufficient freezing for useful sample recovery is time consuming, the deep-sea freezer opens a whole frontier of new possibilities for preserving various types of deep-sea samples and has the potential to be adapted according to various needs of the deep-sea research community. With the first literal ‘marine snow’ in the deep, we offer a glimpse to a future where the recovery of reliable bathyal samples is no longer laborious

Degradation and alteration of phytodetritus by benthic foraminifera: in situ 13C-tracer experiments

Abstrac

In Search of a Sustainable Global Agri-Food System

The potential to meet global food demand fully exists through global development of the high-technology (HT), high-intensity type of agriculture and food processing system prevailing in developed countries. This system unfortunately is also responsible for much natural resource degradation, environmental damage and ecological imbalance. Meantime the Earth's human population continues to grow, placing ever-increasing demand on global natural resources, not only for food but also for living and recreational space. A more sustainable agri-food system must evolve. Sustainability is complex, and ought to be approached from a multidisciplinary perspective and compromise sought in resolving the obvious conflicts amongst biological, environmental, ecological, socio-economic, and other individual disciplines and competing philosophies. These form the basis for comparing three different agricultural production systems: high technology (HT); reduced input (RI), and organic (ORG). The three systems are compared empirically using primary data from farms in each group in southern Ontario, Canada. HT systems prevalent in Canada is highly productive, but its sustainability is questionable. It was concluded that the HT system should not be the model for the future. The ORG system is the least inimical to the environment, ecology, and human operators. It was concluded that the ORG system is sustainable except for its requirement for extensive use of land. The RI system causes minimal environmental and ecological damage. It is most profitable and is supportive of rural farm community viability. It was concluded that the RI system holds the best potential for meeting overall sustainability for the global agri-food system.Farm Management, Land Economics/Use,

Intracellular isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments : results of nitrate and sulfate labeling experiments

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 7 (2016): 163, doi:10.3389/fmicb.2016.00163.Some benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation with isotopically labeled nitrate and sulfate in dysoxic or anoxic conditions. After 2 weeks of incubation, foraminiferal specimens were fixed and prepared for Transmission Electron Microscopy (TEM) and correlative nanometer-scale secondary ion mass spectrometry (NanoSIMS) analyses. TEM observations revealed that there were characteristic ultrastructural features typically near the cell periphery in the youngest two or three chambers of the foraminifera exposed to anoxic conditions. These structures, which are electron dense and ~200–500 nm in diameter and co-occurred with possible endobionts, were labeled with 15N originated from 15N-labeled nitrate under anoxia and were labeled with both 15N and 34S under dysoxia. The labeling with 15N was more apparent in specimens from the dysoxic incubation, suggesting higher foraminiferal activity or increased availability of the label during exposure to oxygen depletion than to anoxia. Our results suggest that the electron dense bodies in Ammonia sp. play a significant role in nitrate incorporation and/or subsequent nitrogen assimilation during exposure to dysoxic to anoxic conditions.This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (Young Scientists B No. 22740340 and Scientific Research C No. 24540504 to HN), an Invitation Fellowship for Research in Japan to JB by Japan Society for the Promotion of Science (JSPS), the Robert W. Morse Chair for Excellence in Oceanography at WHOI to JB, and The Investment in Science Fund at WHOI to JB

Nutritional sources of meio- and macrofauna at hydrothermal vents and adjacent areas: Natural-abundance radiocarbon and stable isotope analyses

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Nomaki, H., Uejima, Y., Ogawa, N. O., Yamane, M., Watanabe, H. K., Senokuchi, R., Bernhard, J. M., Kitahashi, T., Miyairi, Y., Yokoyama, Y., Ohkouchi, N., & Shimanaga, M. Nutritional sources of meio- and macrofauna at hydrothermal vents and adjacent areas: Natural-abundance radiocarbon and stable isotope analyses. Marine Ecology Progress Series, 622, (2019): 49-65, doi:10.3354/meps13053.Deep-sea hydrothermal vents host unique marine ecosystems that rely on organic matter produced by chemoautotrophic microbes together with phytodetritus. Although meiofauna can be abundant at such vents, the small size of meiofauna limits studies on nutritional sources. Here we investigated dietary sources of meio- and macrofauna at hydrothermal vent fields in the western North Pacific using stable carbon and nitrogen isotope ratios (δ13C, δ15N) and natural-abundance radiocarbon (Δ14C). Bacterial mats and Paralvinella spp. (polychaetes) collected from hydrothermal vent chimneys were enriched in 13C (up to -10‰) and depleted in 14C (-700 to -580‰). The δ13C and Δ14C values of dirivultid copepods, endemic to hydrothermal vent chimneys, were -11‰ and -661‰, respectively, and were similar to the values in the bacterial mats and Paralvinella spp. but distinct from those of nearby non-vent sediments (δ13C: ~-24‰) and water-column plankton (Δ14C: ~40‰). In contrast, δ13C values of nematodes from vent chimneys were similar to those of non-vent sites (ca. -25‰). Results suggest that dirivultids relied on vent chimney bacterial mats as their nutritional source, whereas vent nematodes did not obtain significant nutrient amounts from the chemolithoautotrophic microbes. The Δ14C values of Neoverruca intermedia (vent barnacle) suggest they gain nutrition from chemoautotrophic microbes, but the source of inorganic carbon was diluted with bottom water much more than those of the Paralvinella habitat, reflecting Neoverruca’s more distant distribution from active venting. The combination of stable and radioisotope analyses on hydrothermal vent organisms provides valuable information on their nutritional sources and, hence, their adaptive ecology to chemosynthesis-based ecosystems.We are grateful to the crews and scientists of the R/V ‘Natsushima’ and the ROV ‘Hyper-Dolphin’ of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) during the NT12-10, NT13-09 and NT14-06 cruises, and the R/V ‘Kaimei’ and the KM-ROV of JAMSTEC during the KM-ROV training cruise. We thank Yuki Iwadate for her help on sample preparations and 2 anonymous reviewers and the editor, who provided helpful comments on an earlier version of this manuscript. This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (Scientific Research C 26440246 to M.S.), the Japan Society for the Promotion of Science (Invitational fellowships for research in Japan, S14032 to J.M.B.), the WHOI Robert W. Morse Chair for Excellence in Oceanography, and The Investment in Science Fund at WHOI

Meiofauna in the southeastern Bering Sea: community composition and structuring environmental factors

The Bering Sea is the second largest marginal sea in the North Pacific and is one of the areas with highest biological productivity in high-latitude waters. The continental shelf of the Bering Sea hosts large populations of marine mammals and fishery resources. However, the smaller organisms in benthic ecosystems, including meiofauna, have been largely overlooked in this area, despite their potential importance in ecosystem functioning and the resultant biogeochemical cycles. This study analyzed spatial differences in the total abundance and community structure of the metazoan meiofauna at five stations around the Bering Canyon, located at the southeastern margin of the Bering Sea. Their association with environmental factors in sediments was also studied. The results confirmed that the investigated stations had meiofaunal standing stocks that were comparable to those of other Arctic seas. Among the investigated sediment biological and geochemical parameters (total organic carbon, median grain size, prokaryotic cell numbers, etc.), multivariate analyses showed that the C/N of organic matter in sediments was the main factor associated with meiofaunal community structure