Nanophytobenthos: A Neglected Size Fraction of Marine Benthic Community Studies

Figure 1:Nanophytobenthos (nanobenthic diatoms) of the northern coastal waters of the Yucatán Peninsula: A- Psammodictyon panduriforme (W. Gregory) D. G. Mann, cell length (L)=16μm; B- Nitzschia cf. perminuta Grunow, L=10μm; C- Amphora sp., L=5.5μm; D- Resting spores of the planktonic centric diatom Chaetoceros sp. or Bacteriastrum sp., 7.0-7.6μm in diameter; E- (?)Amphora sp., L=19μm; F- The same (?)Amphora sp. (in the left lower corner) as in Fig. E, in comparison to another larger pennate diatom, L=82μm.

In marine costal zones, a variety of organisms contribute to the primary productivity of the ecosystems around the world: sea grasses, macroalgae, mangroves, planktonic and benthic microalgae, cyanobacteria (sometimes considered as microalgae or even macroalgae if visible without a microscope), photosynthetic ciliates and some others. In the sea, two taxonomic groups, diatoms (Bacillariophyceae) and dinoflagellates (Dinophyceae), predominate in phytoplankton in terms of cell abundance and species richness. In benthic environments, diatoms are far more diverse than dinoflagellates. The classification of plankton into different size fractions by Sieburth et al. [1] has been widely accepted; however, that is not the case for the small size fractions of benthic organisms. As applied to planktonic algae, the terms “microplanktonic”, “nanoplanktonic” and “picoplanktonic” are common in the published literature. The term “microphytobenthos” is also commonly used. However, the term “nanophytobenthos” is almost impossible to find. Among benthic diatoms, which belong to the microphytobenthos, nanobenthic species are also common. Although the aforementioned classification considers only planktonic organisms, it is logical to follow it by distinguishing different size fractions within the phytobenthos. Thus, microalgal cells of 2 to 20μm in length should be considered nanophytobenthos, and the diatom cells within this size range would be nanobenthic diatoms. They are represented predominantly by pennate forms (Figure 1A-C, E&F), but also by centric vegetative cells and resting spores (Figure 1D).

Benthic or epibenthic assemblages (sometimes also called communities) include sand-dwelling (interstitial), epilithic, epizoic and epiphytic species. Most benthic microalgae and protozoans have cell sizes ranging from 20 to 200μm and constitute the microbenthos, similar to those inhabiting the water column, which are classified as microplankton [1]. In coastal marine tropical waters, microphytobenthos mainly consists of pennate diatoms, cyanobacteria and dinoflagellates; these are almost exclusively unicellular organisms represented by solitary cells or united into colonies. For example, in Mexican coastal waters, 1162 marine benthic diatom species and infraspecific taxa have been reported [2]. As for marine benthic dinoflagellates, 242 species from 63 genera are known globally [3].

Benthic diatoms show a wide variation in cell size. A series of binary asexual divisions of diatom cells results in reducing the cell size in a local population because the epivalve and hypovalve of the mother cell become epivalves of the two daughter cells, so that a larger part of the cells after recurrent division form a hypovalve that is smaller than the epivalve. Therefore, some cells can be classified as microphytobenthos (>20μm) and others as nanophytobenthos (<20μm) because of the cell length variability range.

Ultrastructural (performed primarily using a transmission electron microscope), biochemical and molecular-genetic studies of microalgae have allowed taxonomists to describe new classes, orders and divisions. Small-sized phytoflagellates still remain a challenge for taxonomists and ecologists. In Italian coastal waters, referring to them as ultraphytoplankton (autotrophic eukaryotic cells of <5μm), Cryptophyceae, Chrysophyceae, Prymnesiophyceae, Pelagophyceae, Dictyochophyceae, Bacillariophyceae and Prasinophyceae have been found using genetic methods [4]. Among picoplanktonic organisms, cyanobacteria were found to be dominant in tropical waters [5]. The genera of photosynthetic bacteria Prochlorococcus Chisholm et al. [6] and Synechococcus Nägeli were found to be the most abundant primary producers in the oceanic zone [7]. In some regions of the world’s oceans, picoplanktonic algae, both prokaryotic and eukaryotic, have been recognized as important primary producers in the water column [8,9]. In particular, many studies on the prokaryotic Prochlorophyta have been performed [6,10-14] (for more references, see [15]). In Japanese coastal waters, cyanobacteria were responsible for 73- 99% of the total picoplankton cell abundance during the entire year [15]. Compared to the aforementioned advances in picoplankton studies started in the late 1970’s [16-18], we must admit that the diversity and ecological roles of the nanophytobenthos are as yet unrevealed.

My sincere thanks go to Dora A. Huerta-Quintanilla (Centro de Investigación y Estudios Avanzados – Instituto Politécnico Nacional (CINVESTAV-IPN), Unidad Mérida, Mérida, Yucatán, Mexico) for her technical assistance with a JEOL JSM-7600F field emission scanning electron microscope, to Francisco O. López-Fuerte (Universidad Autónoma de Baja California Sur, La Paz, B.C.S., Mexico) for his help in identifying benthic diatoms, and to Natalia A. Okolodkova (Mexico City, Mexico) and Ana E. Ramos-Santiago (IPN-CICIMAR, La Paz, B.C.S., Mexico) for their technical help with the figures. This study was partially supported by FOMIX-YUC No. 108160 (2008) and CONACYT LAB-2009-01 No. 123913 (2009) projects led by Patricia Quintana-Owen (CINVESTAV-IPN). Marcia M. Gowing (Seattle, WA, U.S.A.) kindly improved the writing style.

1. Sieburth JMcN, Smetacek V, Lenz V (1978) Pelagic ecosystem structure: Heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography 23(6): 1256-1263.
2. López-Fuerte FO, Siqueiros-Beltrónes D (2016) A checklist of marine benthic diatoms (Bacillariophyta) from Mexico. Phytotaxa 283(3): 201-258.
3. Hoppenrath M, Chomérat N, Horiguchi T, Murray SA, Rhodes L (2023) Marine benthic dinoflagellates: Their relevance for science and society (2^nd edn), E. Schweizerbart’sche Publishing House (Nägele and Obermiller) and Senckenberg Society for Natural Research, Germany, pp. 1-376.
4. McDonald SM, Sarno D, Scanlan DJ, Zingone A (2007) Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquatic Microbial Ecology 50(1): 75-89.
5. Murphy LS, Haugen EM (1985) The distribution and abundance of phototrophic ultraplankton in the North Atlantic. Limnology and Oceanography 30(1): 47-58.
6. Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, et al. (1992) Prochlorococcus marinus gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Archives of Microbiology 157: 297-300.
7. Azam F, Worden AZ (2004) Microbes, molecules, and marine ecosystems. Science 303(5664): 1622-1624.
8. Platt T, Subba Rao DV, Irwin B (1983) Photosynthesis of picoplankton in the oligotrophic ocean. Nature 301(5902): 702-704.
9. Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, et al. (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343.
10. Lewin RA (1975) A marine Synechocystis (Cyanophyta, Chroococcales) epizoic on ascidians. Phycologia 14(3): 153-160.
11. Lewin R (1976) Prochlorophyta as a proposed new division of algae. Nature 261(5562): 697-698.
12. Lewin R (2002) Prochlorophyta – a matter of class distinctions. Photosynthesis Research 73(1-3): 59-61.
13. Olson RJ, Chisholm SW, Zettler ER, Altabet MA, Dusenberry JA (1990) Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep-Sea Research 37(6): 1033-1051.
14. Urbach E, Robertson DL, Chisholm SW (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355(6357): 267-270.
15. Miyazono A, Odate T, Maita Y (1992) Seasonal fluctuations of cell density of cyanobacteria and other picophytoplankton in Iwanai Bay, Hokkaido, Japan. Journal of Oceanography 48: 257-266.
16. Johnson PW, Sieburth JMN (1979) Chroococcoid cyanobacteria in the sea: A ubiquitous and diverse phototropic biomass. Limnology and Oceanography 24(5): 928-935.
17. Johnson PW, Sieburth JMN (1982) In-situ morphology and occurrence of eukaryote phototrophs of bacterial size in the picoplankton of estuarine and oceanic waters. Journal of Phycology 18(3): 318-327.
18. Waterbury JB, Watson SW, Guillard RRL, Brandt LE (1979) Widespread occurrence of a unicellular, marine, planktonic cyanobacterium. Nature 277: 293-294.