ArticlePDF Available

Heterotrophic flagellates and other protists associated with oceanic detritus throughout the water column in the mid North Atlantic

DOI:10.1017/S0025315400032653
Authors:
David Patterson at Maple Ferryman
David Patterson
  • Maple Ferryman
Kari Nygaard
Kari Nygaard
Kari Nygaard
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Gero Steinberg at University of Exeter
Gero Steinberg
Carol Mary Turley at Plymouth Marine Laboratory
Carol Mary Turley
Download full-text PDFDownload full-text PDFDownload full-text PDF
Read full-text
Download citation

Abstract

Heterotrophic protists, mostly flagellates, encountered in association with marine detritus from various collections in the mid North Atlantic are described. About 40 species have been identified and are reported. Taxa reported here for the first time are: Caecitellus gen. nov. (Protista incertae sedis) and Ministeria marisola gen. nov., sp. nov. (Protista incertae sedis). The flagellates form a subset of the community of heterotrophic marine flagellates encountered in more productive marine sites. Most species are bacterivorous and small. The community extends to the ocean floor but the diversity is reduced in samples taken from greater depths. The decline in species diversity is linked also to a decline in numbers of individuals. We discuss these changes in relation to food supply and pressure effects.
Patterson et al._1993_J. mar. biol Ass. U.K
.73_67.pdf
Content uploaded by Gero Steinberg
Author content
All content in this area was uploaded by Gero Steinberg on Jun 21, 2015
Content may be subject to copyright.
Patterson et al._1993_J. mar. biol Ass. U.K
.73_67.pdf
Content uploaded by Gero Steinberg
Author content
All content in this area was uploaded by Gero Steinberg on Jun 21, 2015
Content may be subject to copyright.
Patterson et al._1993_J. mar. biol Ass. U.K
.73_67.pdf
Content uploaded by Gero Steinberg
Author content
All content in this area was uploaded by Gero Steinberg on Jun 21, 2015
Content may be subject to copyright.
A preview of the PDF is not available
... Faunistic investigations of heterotrophic flagellates and heliozoans supported with morphological descriptions were especially common in protistological literature in the 90 s -early 2000s (Larsen and Patterson 1990; Lee and Patterson 2000;Lee et al. 2003;Mikrjukov 2001;Patterson and Simpson 1996;Patterson et al. 1993;Tong 1997b, c;Vørs 1992). At present, such studies are relatively rare and have been largely replaced by molecular surveys from bulk microbial community DNA (Geisen et al., 2019;Pawlowski et al., 2016). ...
... Distribution: Marine waters of Australia (Tong et al. 1998), Brazil (Larsen and Patterson 1990), U.K. (Patterson et al. 1993;Tong 1994Tong , 1997c. ...
Heterotrophic flagellates and centrohelid heliozoans from marine waters of Curacao, the Netherlands Antilles
Article
Recent progress in understanding the early evolution of eukaryotes was tied to morphological identification of flagellates and heliozoans from natural samples, isolation of their culture and genomic and ultrastructural investigations. These protists are the smallest and least studied microbial eukaryotes but play an important role in the functioning of microbial food webs. Using light and electron microscopy, we have studied the diversity of heterotrophic flagellates and centrohelid heliozoans from marine waters of Curacao (The Netherlands Antilles), and provide micrographs and morphological descriptions of observed species. Among 86 flagellates and 3 centrohelids encountered in this survey, five heterotrophic flagellates and one сentrohelid heliozoan were not identified even to the genus. Some flagellate protists have a unique morphology, and may represent undescribed lineages of eukaryotes of high taxonomic rank. The vast majority (89%) of identified flagellates is characterized by wide geographical distribution and have been reported previously from all hemispheres and various climatic regions. More than half of the species were previously observed not only from marine, but also from freshwater habitats. The parameters of the species accumulation curve indicate that our species list obtained for the Curacao study sites is far from complete, and each new sample should yield new species.
... Heterotrophic protists play an essential role as they remineralize nutrients from bacterial and phytoplankton production and provide them to higher trophic levels (Massana et al., 2009;Pernthaler, 2005). Exemplified by studies from the Atlantic Ocean, only few approaches have been attempted to study the abundance (Mangot et al., 2018), taxonomic composition (Countway et al., 2007), distribution (de Vargas et al., 1999) and diversity (Patterson et al., 1993) of heterotrophic flagellates in the off-shelf waters. Most studies focused on neritic pelagic zones (Bergesch et al., 2008;Gran-Stadniczeñko et al., 2019), which differ in their community composition compared to pelagic oceanic habitats. ...
Controls in benthic and pelagic BIODIversity of the Azores – BIODIAZ
Conference Paper
  • Feb 2022
METEOR Cruise M150 BIODIAZ provided material from sublittoral down to deep-sea stations to incorporate innovative aspects into the study of seamount and island productivity and their potential role for the establishment of benthic assemblages comprising all size classes (George et al. 2021). The aim was to get a baseline on the diversity, faunal composition and distribution of shelf and deep-sea taxa and related sediments from three different Azorean islands (Flores, Terceira, and Santa Maria) and two adjacent seamounts (Princess Alice Bank, Formigas Bank). Such baseline shall serve to prove fundamental hypotheses regarding the role of seamounts/islands for marine organisms and the principle (bio)-sedimentary processes in the evolution of seamounts. The significance of potential endemism in zoobenthic communities based on the extensively sampled material is studied in the context of the geologic age, topographic isolation, phytoplankton productivity and diversity of the systems.
... The important role of protists in energy transfer through aquatic food webs has been well established for shallow benthic and pelagic marine ecosystems 12,13 , where protists have developed a wide range of nutritional strategies 14 . Within the euphotic water column, marine photosynthetic plankton forms the base of ocean food webs having a profound influence on the global carbon cycle. ...
High and specific diversity of protists in the deep-sea basins dominated by diplonemids, kinetoplastids, ciliates and foraminiferans
Article
Full-text available
  • Apr 2021
Heterotrophic protists (unicellular eukaryotes) form a major link from bacteria and algae to higher trophic levels in the sunlit ocean. Their role on the deep seafloor, however, is only fragmentarily understood, despite their potential key function for global carbon cycling. Using the approach of combined DNA metabarcoding and cultivation-based surveys of 11 deep-sea regions, we show that protist communities, mostly overlooked in current deep-sea foodweb models, are highly specific, locally diverse and have little overlap to pelagic communities. Besides traditionally considered foraminiferans, tiny protists including diplonemids, kineto-plastids and ciliates were genetically highly diverse considerably exceeding the diversity of metazoans. Deep-sea protists, including many parasitic species, represent thus one of the most diverse biodiversity compartments of the Earth system, forming an essential link to metazoans.
... Kinetoplastids are very numerous in benthic communities, where they constitute 5-20% of the total biomass of all heterotrophic flagellates, second only to euglenids, suggesting their important role in controlling bacterial growth [42]. They are abundant in seawater ice and some species can be cultured even from the pelagic zone, demonstrating their presence there at least at the cystic stage [43,44]. Recent studies using molecular methods demonstrated that in many water bodies, most of the kinetoplastid biomass is created by neobodonids, of which Neobodo, Rhynchomonas and Dimastigella are the most frequent ones ( plate A, 7,9,14) [45][46][47]. ...
Euglenozoa: Taxonomy, diversity and ecology, symbioses and viruses
Article
Full-text available
  • Mar 2021
Euglenozoa is a species-rich group of protists, which have extremely diverse lifestyles and a range of features that distinguish them from other eukar-yotes. They are composed of free-living and parasitic kinetoplastids, mostly free-living diplonemids, heterotrophic and photosynthetic euglenids, as well as deep-sea symbiontids. Although they form a well-supported monophyletic group, these morphologically rather distinct groups are almost never treated together in a comparative manner, as attempted here. We present an updated taxonomy, complemented by photos of representative species, with notes on diversity, distribution and biology of euglenozoans. For kinetoplastids, we propose a significantly modified tax-onomy that reflects the latest findings. Finally, we summarize what is known about viruses infecting euglenozoans, as well as their relationships with ecto-and endosymbiotic bacteria.
... Hence, our data might imply increased virusdriven lysis of prokaryotes with increasing water depth. This explanation aligns with previous studies arguing that low prokaryotic abundances make eukaryotic grazing energetically unfavorable, thus reducing energy transport to higher trophic levels and leaving viruses as the dominant mortality factor for prokaryotes in low cell density environments (Patterson et al. 1993;Magagnini et al. 2007;Pachiadaki et al. 2016). ...
Spatial variability of prokaryotic and viral abundances in the Kermadec and Atacama Trench regions
Article
Full-text available
Hadal trenches represent the deepest part of the ocean and are dynamic depocenters with intensified prokaryotic activity. Here, we explored the distribution and drivers of prokaryotic and viral abundance from the ocean surface and 40 cm into sediments in two hadal trench regions with contrasting surface productivity. In the water column, prokaryotic and viral abundance decreased with water depth before reaching a rather stable level at ~ 4000 m depth at both trench systems, while virus to prokaryote ratios were increasing with depth, presumably reflecting the declining availability of organic material. Prokaryotic and viral abundances in sediments were lower at the adjacent abyssal sites than at the hadal sites and declined exponentially with sediment depth, closely tracking the attenuation of total organic carbon (TOC) content. In contrast, hadal sediment exhibited erratic depth profiles of prokaryotes and viruses with many subsurface peaks. The prokaryotic abundance correlated well to extensive fluctuations in TOC content at centimeter scale, which were likely caused by recurring mass wasting events. Yet while prokaryotic and viral abundances cross correlated well in the abyssal sediments, there was no clear correlation in the hadal sites. The results suggested that dynamic depositional conditions and higher substrate availability result in a high spatial heterogeneity in viral and prokaryotic abundances in hadal sediments in comparison to more stable abyssal settings. We argue that these conditions enhance the relatively importance of viruses for prokaryotic mortality and carbon recycling in hadal settings.
... With regard to POC, other non-diatom phytoplankton groups may also be incorporated into sinking marine aggregates as components of the export flux (e.g. Patterson et al., 1993;Durkin et al., 2016). Although these organisms, such as dinoflagellates, naked nanoflagellates, or cyanobacteria, are not well preserved in the sediment traps they are often more abundant north of the STFZ (Chang and Gall 1998;Hawes et al., 1997;Gall et al., 1999) and could contribute to export fluxes in this region. ...
Diatom and coccolithophore species fluxes in the Subtropical Frontal Zone, east of New Zealand
Article
The Chatham Rise supports some of New Zealand's most economically valuable commercial fish stocks, fuelled by the highly productive waters of the Subtropical Frontal Zone (STFZ). Climate change-related shifts in phytoplankton community structure and function are predicted and may affect Chatham Rise productivity and deep-sea carbon sequestration by the biological carbon pump. However, little is known about how two major phytoplankton groups, diatoms and coccolithophores, will respond, since the seasonality of their productivity and export fluxes to the seafloor are not well known in the SW Pacific sector. This study is the first to report on the seasonal cycle of phytoplankton species fluxes in the STFZ, using a 12-month sediment trap record (1996–1997) on the northern (subtropical-influenced) and southern (subantarctic-influenced) flanks of the Chatham Rise. Diatom and coccolith flux assemblages were characterised and compared with biogeochemical fluxes from the same sites over the same time-frame. Northern phytoplankton flux composition was typical of the subtropics, with most particulate organic carbon (POC) and biogenic silica export associated with diatom fluxes. Fluxes to the northern trap were largely composed of coastal and benthic diatom taxa, reinforcing previous interpretations suggesting lateral advection and sediment resuspension along and across the Chatham Rise slope, influenced also by the Wairarapa Eddy. At the southern site, phytoplankton fluxes were on average an order of magnitude higher than at the northern site and comprised a combination of subantarctic and frontal zone diatom taxa. The majority of the annual diatom flux in the southern trap occurred during a spring Pseudo-nitzschia “pulse” associated with high biogenic silica and POC fluxes, which are inferred to be from subsurface chlorophyll maxima. High coccolith flux at the southern STFZ site was consistent with ecosystem processes observed from other subantarctic export regimes. Phytoplankton successions inferred from the sediment trap records suggest that coccolithophores precede diatoms in spring, which is contrary to expectations from classical studies where the opposite temporal trend is suggested. While maximum diatom species flux co-occurred with peak POC flux at both sites in spring, the estimated contribution of organic carbon associated with diatoms to POC flux was negligible (<0.05%). Estimated coccolithophore POC flux was also low, suggesting that either other phytoplankton groups and/or zooplankton-mediated processes (e.g. fecal pellet fluxes) must contribute more substantially to POC export in the STFZ. Our findings provide new insights into phytoplankton export flux pathways to the seafloor in the Chatham Rise region, with implications for regional biogeochemistry, paleoceanographic and export modelling studies.
... Well-marked 608 ingestion organelle with two gradually narrowing rods extends along entire cell length. Nucleus (Patterson et al. 1993;Tong 1994Tong , 1997c. 652 Skuja, 1948 c (Fig. 5n, o) Cell length is 4.5-5.5 μm, cell width is 3.8-5.5 μm. ...
Heterotrophic flagellates and centrohelid heliozoans from marine waters of Curacao, the Netherlands Antilles
Preprint
Full-text available
  • Aug 2020
Recent progress in understanding the early evolution of eukaryotes was tied to morphological identification of flagellates and heliozoans in the natural samples, isolation of their cultures and genomic and ultrastructural investigations. These protists are the smallest and least studied microbial eukaryotes but play an important role in functioning of microbial food webs. Using light and electron microscopy, we have studied the diversity of heterotrophic flagellates and centrohelid heliozoans from marine waters of Curacao (The Netherlands Antilles), and provide micrographs and morphological descriptions of observed species. Among 86 flagellates and 3 centrohelids encountered in this survey, five heterotrophic flagellates and one сentrohelid heliozoan were not identified even to the genus. Some flagellate protists have a unique morphology, and may represent undescribed lineages of eukaryotes of high taxonomic rank. The vast majority (89%) of identified flagellates are characterized by wide geographical distribution and had been reported previously from all hemispheres and various climatic regions. More than half of the species were previously observed not only from marine, but also from freshwater habitats. The parameters of the species accumulation curve indicate that our species list obtained for the Curacao study sites is far from complete, and each new sample should yield new species.
Cafeteria in extreme environments: investigations on C. burkhardae and three new species from the atacama desert and the deep ocean
Article
The heterotrophic nanoflagellate genus Cafeteria has been found to be ubiquitously distributed in the marine realm. We could isolate and cultivate ten strains morphologically similar to Cafeteria from various types of environment, including the deep sea, brackish waters and also meso- to hypersaline inland waters. Molecular analyses (18S rDNA, 28S rDNA) of newly isolated strains from the marine realm resulted in four more Cafeteria burkhardae strains from the deep North Atlantic Ocean and one new species (C. baltica sp. nov.) isolated from brackish waters of the Baltic Sea. Two strains isolated from the Atacama Desert belong to two new species (C. atacamiensis sp. nov. and C. paulosalfera sp. nov.), one other strain could not yet be assigned. Morphological characterizations of these strains obtained by high resolution microscopy revealed only small differences to already described species. However, molecular analyses showed a clear separation of the different Cafeteria species. We exposed several strains to different salt concentrations (2-150 PSU) to investigate their salinity tolerance. Only the marine strains of C. burkhardae were able to survive at salinities up to 150 PSU, indicating the possibility to inhabit a broader spectrum of habitats including hypersaline environments besides the deep sea with its high hydrostatic pressure.
Txikispora philomaios n. sp., n. g., a Micro‐Eukaryotic Pathogen of Amphipods, Reveals Parasitism and Hidden Diversity in Class Filasterea
Article
  • Nov 2021
This study provides a morphological, ultrastructural, and phylogenetic characterization of a novel micro-eukaryotic parasite (2.3-2.6 µm) infecting amphipod genera Echinogammarus and Orchestia. Longitudinal studies across two years revealed that infection prevalence peaked in late April and May, reaching 64% in Echinogammarus sp. and 15% in Orchestia sp., but was seldom detected during the rest of the year. The parasite infected predominantly haemolymph, connective tissue, tegument, and gonad, although hepatopancreas and nervous tissue were affected in heavier infections, eliciting melanization and granuloma formation. Cell division occurred inside walled parasitic cysts, often within host haemocytes, resulting in haemolymph congestion. Small subunit (18S) rRNA gene phylogenies including related environmental sequences placed the novel parasite as a highly divergent lineage within Class Filasterea, which together with Choanoflagellatea represent the closest protistan relatives of Metazoa. We describe the new parasite as Txikispora philomaios n. sp. n. g., the first confirmed parasitic filasterean lineage, which otherwise comprises four free-living flagellates and a rarely observed endosymbiont of snails. Lineage-specific PCR probing of other hosts and surrounding environments only detected T. philomaios in the platyhelminth Procerodes sp. We expand the known diversity of Filasterea by targeted searches of metagenomic datasets, resulting in 13 previously unknown lineages from environmental samples.
Loricate choanoflagellates (Acanthoecida) from warm water seas. VIII. Crinolina Thomsen and Diaphanoeca Ellis
Article
Full-text available
The loricate choanoflagellate genera Diaphanoeca Ellis and Crinolina Thomsen encompass a total of ten species. The majority of these are recorded from the warm water regions reported on here. A distinct morphological dichotomy characterizes the genus Diaphanoeca as currently circumscribed. The species distribute themselves within a ‘D. grandis subgroup’ and a ‘D. pedicellata subgroup’ distinguished on e.g., the position of the protoplast inside the lorica chamber and the elaboration of the anterior projections. We are, while awaiting in particular further molecular evidence, taking a conservative approach and abstain from dealing with the subgroup issue at the generic level. The examination of material from the warm water regions of the world’s oceans has resulted in the description of D. sargassoensis sp.n., D. pseudoundulata sp.n., and D. throndsenii sp.n., and a thorough re-examination of D. undulata. Species of Crinolina share multiple features with in particular the D. grandis species subgroup. It is yet relevant, both in a morphological and molecular perspective, to retain the genus Crinolina which remains unambiguously defined based on the posteriorly open lorica. A high level of agreement is found when contrasting morphological and molecular based phylogenetic schemes.
Functional biology of the choanoflagellate Diaphanoeca grandis Ellis
Article
Full-text available
  • Jan 1989
Marine planktonic Acanthoecaceans (Craspedophyceae) from Arctic waters
Article
Choanoflagellate diversity with particular emphasis on the Acanthoecidae. In
Article
  • Jan 1991
Heterotrophic flagellates of uncertain taxonomic position. In
Article
  • Jan 1991
Heterotrophic flagellates of planktonic communities, their characteristics and methods of study
Article
  • Jan 1991
Fine-structural observations on six species of Chrysochromulina from wild Danish marine nanoplankton, including a description of C. campanulifera sp. nov. and a preliminary summary of the nanoplankton as a whole
Article
  • Jan 1974
Characteristic features of the ultrastructure of colourless flagellate Heteromita sp.
Article
  • Jan 1990
Loricate and scale bearing protists from Lützow-Holm Bay, Antarctica II. Four marine species of Paraphysomonas (Chrysophyceae) including two new species from the fast-ice covered coastal areas
Article
  • Jan 1987
Protozoa Associated with Marine ‘Snow’ and ‘Fluff’ — Session Summary
Chapter
  • Jan 1991
The session opened with a brief kaleidoscopic introduction to marine ‘snow’ and ‘fluff’ prior to the key note address by Karin Lochte (1990). Points of particular interest have been highlighted from the introduction, the contributed papers and the discussion forum.
Recent researches on the Choanoflagellata (Craspedomonadines) (freshwater and marine) with description of new genera and species
Article